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Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs

Article  in  Limnology and Oceanography · July 1997

DOI: 10.4319/lo.1997.42.5_part_2.1203


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I.~miml Ocmrogr.. 42(5, part 2), 1997, 1203-1214
64 1997, 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

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

Toxic or otherwise harmful phytoplankton blooms may be phytoplankton blooms may have conferred some ability to
increasing in frequency worldwide (Smayda 1989; Hallegracff consume toxic phytoplankton with no ill effects.
1993). Accumulation of phytoplankton toxins in shellfish with Much of the disparity of effects is due to the variety of
subsequent poisoning of humans (Shumway 1990) and fish phytoplankton toxins. Among the approximately 20 phyto-
kills (Steidinger 1983; Burkholder et al. 1995) are widely plankton genera known to be toxic (Taylor 1990), there is a
known, However, interactions between toxic phytoplankters plethora of toxins with widely differing effects (see Steidin-
and their zooplankton grazers, subsequent food-web transport ger 1983; Baden and Trainer 1993; Hallegraeff 1993) which
of toxins, and effects on pelagic consumers at higher trophic can vary with potency and concentration (Anderson et al.
levels are more obscure. Phycotoxin transport through food 1990, 1994; Cembella et al. 1988). Intracellular levels of
webs is indicated by mortality of whales, dolphins, and sea toxins can vary within a single algal clone, depending upon
birds following ingestion of phycotoxins (Anderson and White culture age and conditions (Maranda et al. 1985; Baden and
1992; Gerachi et al. 1989; Work et al. 1993). Tomas 1988; Cembella and Therriault 1989; Bates et al.
The reasons for phytoplankton toxin production are not 1991, 1993; Flynn and Flynn 1995; see also Graneli et al.
clear. Just because phytoplankters are toxic dots not mean 1990; Smayda and Shimizu 1993; Lassus et al. 1995) or
neccessarily that toxicity evolved to repel grazers. Indeed, presence of toxic intracellular bacteria (Kodama 1990; Dou-
certain zooplankton ingest various toxic phytoplankters with cette 1995). Variations in phytoplankton toxicity result in
impunity, whereas for others, deleterious effects may result. complex and inconsistent interactions between toxic phyto-
Putative explanations for toxicity other than grazing deter- plankters and their grazers. There is also variation in phys-
rence include precursors for subcellular organelles (Baden et iological responses of organisms to algal toxins in terms of
al. 1979), cell-wall degradation products (Kim and Martin binding or recognition-the initial event in the onset of tox-
1974), nucleic acid synthesis (Abbott and White 1979; icity (Baden and Trainer 1993). Most marine phycotoxins
Yentsch 1981), nitrogen storage (Dale and Yentsch 1978), or influence neurotransmission or enzyme inhibition (Table 1).
inhibition of competing, co-occurring phytoplankton species Differences in affinity of binding sites or the degree of de-
(Freeberg et al. 1979; Windust et al. 1996). Within the phy- centralization of invertebrate nervous systems may account
toplankton-zooplankton community there are few examples for the lack of apparent effect of some toxins.
of toxins as grazing deterrents to compare with the coevo- Beyond effects on their immediate grazers, phytoplankton
lution between benthic marine grazers and antipredatory toxins may be passed up the food web through zooplankton
chemicals in the plants they consume (Hay 1991). There are and fish that serve as vectors for higher trophic levels. Other
only suggestions from studies of copepods (Turner and Test- than for ciguatera fish poisoning, there is little information
er 1989) and bivalve molluscs (Shumway and Cucci 1987) about this process, and it is difficult to assess the potential
that coevolutionary experience or periodic exposure to toxic for toxins reaching fish that could be consumed by humans.
Just as toxic phytoplankters have potential impact on zoo-
plankton and other pelagic consumers, grazing can have po-
Acknowledgments tential impact on preventing or terminating blooms. An ob-
We thank Don Anderson, Dave Garrison, Kevin Sellner, Peter vious implication of a large monospecific bloom is that
Verity, and an anonymous reviewer for constructive criticism of grazing control is out-of-balance with phytoplankton growth
several earlier, longer versions of this review. and(or) physical concentration. Such an occurrence may be
1204 Turner and Tester

Table 1. Characteristics of phytoplankton toxins.

Toxin Mode of action Characteristics

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 fre-
quency of end-plate potentials, ultimately resulting in depletion of neu-
rotransmitted 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 Gambierdis-
cus 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 re-
petitive synaptic stimulation.
Saxitoxin Na+ channel blocker Paralytic shellfish poisons include at least a dozen saxitoxins, neosaxitox-
ins, and gonyautoxins They are produced mainly by members of the
dinoflagellate genera Uexandrium, Gonyaulax, Protogonyaulax, Pyro-
dinium, 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 hu-
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 neu-
ronal 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 spe-
cies 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 toxin Neurotoxicity There is an uncharacterized toxin produced by the dinoflagellate Pjester-
ia 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 en-
zyme levels, high phosphorus excretion, and immune system suppres-
sion. This toxin seems IO have only minimal effects, if any, on the co-
pepod Acartia tonsa or the rotifer Brachionus plicatilis (Mallin et al.

due to poisoning of grazers by phycotoxins, but it may also protists and rotifers, as well as grazing and food-web interactions
be due to low abundances of grazers or other factors. with other toxic nonflagellate phytoplankters.
We review interactions between toxic phytoplankters and their
grazers, and the accumulation and transport of phycotoxins Interactions of toxic phytoplankters with copepods
through pelagic food webs. Most work has focused on grazing and other metazooplankton grazers
of metazoans such as copepods feeding on toxic dinoflagellates
and other flagellates, but there is increasing information on in- Dinoflagellate:: and microjlugellates-Some copepods
teractions between toxic phytoplankters and microzooplanktonic seem adversely affected by toxic dinoflagellates. Effects in-
Toxic algae and grazers 1205

elude reduced feeding, egg production, and survival (Gill the Gulf of Maine feeding on toxic isolates of Alexandrium
and Harris 1987) or avoidance of dinoflagellate-rich layers fundyense and A. tamarense, Teegarden and Cembella (1996)
during blooms (Fiedler 1982; Huntley 1982). found that neither copepod evidenced incapacitation from
A chemical component may cause reduced grazing and toxins, both accumulated toxins, and both grazed toxic and
avoidance behavior. When clones of Alexandrium tamarense nontoxic isolates at high rates. Because responses of the two
that varied in toxicity were fed to the copepods Acartia hud- copepods were different under the same combinations of
sonica and Pseudocalanus sp., ingestion rates decreased with food, or varied with different combinations of food, Teegar-
increasing levels of cellular toxicity (Ives 1985). Copepods den and Cembella concluded that copepod grazing responses
feeding on more toxic clones were paralyzed. Ives (1985, to toxic vs. nontoxic phytoplankters are highly specific for
1987) suggested that chemically induced suppression of particular combinations of predators and prey and that pres-
grazing may be due to behavioral rejection of toxic cells ence or absence or relative potency of toxins are not always
prior to ingestion or ingestion of toxic cells causing pro- the major determinants of any selective feeding response.
gressive paralysis. Ives concluded that physiological inca- Toxic dinoflagellates rarely bloom in nature in the absence
pacitation rather than behavioral rejection of toxic cells was of other phytoplankters so differing responses by various
most likely. grazers to specific combinations of toxic and nontoxic prey
Huntley et al. (1986) tested 13 species or clones of di- likely contribute to differing grazing patterns. Turner and
noflagellates for rejection by the copepods Calanus pacijcus Anderson (1983) found that during spring blooms of A. ta-
and Paracalanus parvus. Five clones were rejected, includ- marense in Cape Cod salt ponds, the copepod A. hudsonica
ing two different clones of A. tamarense and Gymnodinium and planktonic larvae of the polychaete Polydora sp. ate the
breve, Scrippsiella trochoidea, and Protoceratium reticula- toxic dinoflagellate. Feeding rates on the toxic dinoflagellate
turn. P. reticulaturn was repeatedly rejected as food by C. were low because of low ambient temperatures and ingestion
pacijcus. Starved copepods would not feed on it, and co- of more abundant co-occurring tintinnids and the nontoxic
pepods maintained with it ceased reproduction and had high dinoflagellate Heterocapsa triquetra. There were no appar-
mortality. Both cells and filtrate from P. reticulaturn cultures ent adverse effects of ingesting A. tamarense on either co-
reduced feeding on the normally edible dinoflagellate Gy- pepods or polychaete larvae.
rodinium resplendens. Direct observations with video cine- During a massive bloom of the dinoflagellate G. breve off
matography (Sykes and Huntley 1987) revealed that feeding North Carolina in 1987, Turner and Tester (1989) examined
on P. reticulaturn caused reverse peristalsis (“retching”) and grazing on natural water samples by five co-occurring spe-
regurgitation in copepods, and G. breve caused elevated cies of copepods (A. tonsa, Oncaea venusta, Labidocera aes-
heart rate and loss of motor control. Huntley et al. (1986) tiva, Centropages typicus, and Paracalanus quasimodo). All
concluded that a physiological reaction rendered copepods five copepods ingested G. breve, but rates were variable and
incapable of further feeding on P. reticulaturn and G. breve, generally low. Rates of ingestion of G. breve by A. tonsa,
possibly resulting in diminished growth and reproduction, 0. venusta, and L. aestiva increased with increasing natural
eventually causing declines in the abundance of grazers. Be- concentrations of G. breve up to 2X lo4 cells ml-‘, particu-
cause dinoflagellate blooms may last for periods of several larly at levels >3 X 1Oj cells ml- I. C. typicus ingested G.
weeks, effects of both relaxed grazing pressure and lower breve in three of six trials at extremely low rates. P. quas-
fecundity may be contributing factors to the perpetuation of imodo, a small copepod (< 1 mm long), possibly had trouble
toxic blooms. ingesting the large (>30 p,m wide) G. breve, and ate little.
Uncertainty exists as to whether grazing-inhibitory chem- In two of the natural water samples used as food, the diatom
icals are intracellular or extracellular. Heterosigma carterae Skeletonema costatum was abundant; in both cases, ingestion
and Gymnodinium nagasakiense apparently have intracellu- of G. breve by A. tonsa, C. typicus, and L. aestiva dropped
lar compounds (Uye and Takamatsu 1990), but in P. reti- to near zero while rates of ingestion of S. costatum remained
culatum compounds seem to be extracellular (Huntley et al. high. Thus, these copepods ate the toxic dinoflagellate when
1986). Van Alstyne (1986) found that feeding by the cope- presented with essentially nothing else, but given a choice,
pod Centropages hamatus was suppressed by both intra- and did not. Despite this selection against G. breve the copepods
extracellular compounds of H. carterae and intracellular did not seem adversely affected by 18-22-h incubations. Re-
chemicals of S. trochoidea. Uye and Takamatsu (1990) con- cent experiments with concentrations of 10” cells liter-’ in-
cluded that the effects of copepod-flagellate grazing inter- dicate that A. tonsa can accumulate toxins from G. breve,
actions are species-specific. become lethargic, but recover after being placed in filtered
Two recent studies of copepod grazing on unialgal diets seawater (Turner and Tester unpubl. data).
of toxic Alexandrium isolates gave somewhat different re- Failure of C. typicus to ingest G. breve during the 1987
sults. Turriff et al. (1995) examined feeding of Calanus fin- North Carolina bloom suggested the possibility of a biogeo-
marchicus adult females from the St. Lawrence estuary on graphic explanation because C. typicus and G. breve rarely
toxic and nontoxic clones of Alexandrium excavatum. Clear- co-occur in nature. G. breve normally blooms in the Gulf of
ance rates on the nontoxic isolate were high, but near zero Mexico and occasionally in the Atlantic off southeastern
for the toxic strains. When presented with mixtures of non- Florida. Its presence off North Carolina was due to transport
toxic diatoms and toxic dinoflagellates, copepods avoided by the Gulf Stream >lO” km outside its normal range. The
ingesting the dinoflagellates. Although feeding on toxic iso- presence of C. typicus south of Cape Hatteras was also ad-
lates was low, toxins accumulated in the copepods. In a sim- ventitious. This copepod is a regular inhabitant of the cooler
ilar study with Acartia tonsa and Eurytemora herdmani from waters of the mid-Atlantic and New England continental
1206 Turner and Tester

shelves (Turner 198 1) and occurs south of Cape Hatteras There are contradictory results from different copepod
only from late autumn through early spring after northeast feeding studies on the same or different flagellates. For in-
winds push Virginia coastal water southwestward (Bowman stance, H. canerae seemed to be suitable food for A. omorii
1971). Because transport of G. breve via the Gulf Stream (Uye and Tak.amatsu 1990) and C. pacijicus (Sykes and
from the Gulf of Mexico to North Carolina coastal waters Huntley 1987), but not for A. hudsonica and A. tonsa (Tomas
was an unprecedented anomalous hydrographic event (Tester and Deason 1981) or C. hamatus (Van Alstyne 1986). P.
et al. 1989, 1991), both the copepod and the dinoflagellate reticulaturn was rejected by C. pacificus (Huntley et al.
co-occurred in waters regularly inhabited by neither. C. typ- 1986) but not by A. omorii or P. marinus (Uye and Taka-
icus possibly did not eat G. breve because it lacked coevo- matsu 1990).
lutionary experience counteracting toxins of this dinoflagel- The microflagellate C. polylepis caused a large toxic
late. Conversely, the other copepod species that did eat the bloom in Scandinavian waters in May 1988 (Rosenberg et
toxic dinoflagellate regularly coexist with G. breve in coastal al. 1988; Dahl et al. 1989; Graneli et al. 1989; Maestrini and
waters of the Gulf of Mexico. Graneli 1991). Nielsen et al. (1990) found that copepods
If such a biogeographic scenario is valid it may have sev- avoided the dense populations of C. polylepis at the pyc-
eral important implications. First, it suggests caution in in- nocline and copepod egg production rates from this layer
terpreting results of feeding experiments where toxic phy- were lower than for those from above it. In the laboratory,
toplankters from a particular location are fed to grazers from lower clearance, ingestion, and egg production rates resulted
another (Huntley et al. 1986; Ives 1987). Further, because from A. tonsa feeding on C. polylepis when compared to
ballast-water transport inoculates new areas with invading feeding on the same concentrations of a similarly sized non-
species of both dinoflagellates (Hallegraeff 1993) and co- toxic microflagellate Rhodomonas baltica.
pepods (Carlton and Geller 1993), there is a possibility that
introduction of exotic dinoflagellates or copepods could re- Other toxic phytoplankters-Copepod grazing on nonfla-
sult in unprecedented encounters favoring bloom develop- gellated toxic phytoplankters include studies with cyanobac-
ment. teria of the genus Trichodesmium, domoic acid-producing
Toxic dinoflagellates also can have deleterious effects on diatoms of the genus Pseudo-nitzschia, brown tide pico-
copepod developmental stages. Huntley et al. (1987a) found plankters such as Aureococcus anophageflerens, the Texas
that several species of dinoflagellates, including P. reticu- brown tide organism, and intermittently gelatinous and pos-
Zatum and G. breve, were inadequate as food for developing sibly oxic prymnesiophytes of the genus Phaeocystis.
nauplii of C. pacificus. Nauplii feeding only upon these spe- Filamentous cyanobacteria commonly produce nuisance
cies developed at rates similar to starved ones and did not blooms in freshwater and brackish environments (Paerl
molt past the first feeding stage (N3). G. breve caused nau- 1988) and some produce toxins. Filamentous cyanobacteria
plii to lose neuromuscular control, become lethargic, and die. of the genus Trichodesmium are a major component of the
Bagoien et al. (1996) also reported strongly reduced naupliar marine phytoplankton in tropical and subtropical oceans
activity of Euterpina acutifrons after exposure to Alexan- (Carpenter 1983). Although some marine harpacticoid co-
drium minutum and Gymnodinium catenatum. By inhibiting pepods feed on Trichodesmium thiebautii (O’Neil and Ro-
development of copepod nauplii, toxic dinoflagellates may man 1992; Sellner 1992), it is toxic to some Calanoid and
enhance their own survival by suppression of future gener- cyclopoid copepods, brine shrimp, and mice (Hawser et al.
ations of their predators. 1992). Other cy anobacteria blooms (Nodularia spumigena)
There are several studies of copepod grazing on toxic mi- have been associated with mortality of dogs which came in
croflagellates, including the raphidophyceans Chattonella contact with affected water (Edler et al. 1985).
antiqua and H. carterae and the prymnesiophycean micro- Guo and Test’zr (1994) investigated toxicity of Trichodes-
flagellate Chrysochromulina polylepis. Uye (1986) examined mium to the copepod A. tonsa during a natural bloom off
feeding of nine Japanese copepod species on the flagellate North Carolina jn 1992. They found that healthy intact cells
C. antiqua. Three copepod species, thought to be primarily were not toxic to the copepods and were ingested when no
carnivorous, did not ingest C. antiqua and died within sev- other food was available. Conversely, homogenized cells
eral days. The herbivorous copepods fed on the flagellate were lethal to the copepods, suggesting the presence of in-
with no adverse effect. tracellular or cell-wall-bound toxins (Falconer 1993). Guo
Uye and Takamatsu (1990) investigated feeding by the and Tester (199~:) concluded that effects on grazers may de-
copepods Pseudodiaptomus marinus and Acartia omorii on pend on age and physiological state of cells in blooms. Even
red tide dinoflagellates, raphidophytes, prasinophytes, and for copepods which ingested healthy Trichodesmium cells,
euglenophytes. Some dinoflagellates, prasinophytes, and eu- egg production was reduced, suggesting nutritional inade-
glenophytes were “good quality” food for both copepods, quacy or inefficient assimilation.
but other dinoflagellates were good food for one but not the Sellner et al. (1994) also found that cyanobacteria were
other. G. nagasakiense and all rhapidophytes were “poor inadequate food for some zooplankters during cyanobacteria
quality” food for both copepods. These were rejected and blooms in the northern Baltic (Gulf of Finland). The cope-
high mortality and low egg production rates resulted. Uye pods Acartia b$losa and Eurytemora afinis fed on the cy-
and Takamatsu determined that ingestion of the edible di- anobacterium N. spumigena at rates so low that the copepods
noflagellate H. triquetra was inhibited by filtrate from cell were starving, and A. bijilosa had high mortality and gen-
homogenates of rejected algae, indicating that intracellular erally appeared ilnhealthy. In contrast, the cladoceran Bos-
inhibitory chemicals were responsible. mina longispina maritima seemed to ingest large amounts
Toxic algae and grazers 1207

of cyanobacteria, as indicated by cyanobacteria-associated lo-75-fold lower than in comparison years and fewer eggs
pigments in its guts. This was further supported by rapid of the anchovy Anchoa mitchilli (10% of nonbrown tide
movement of cladocerans from cyanobacterial colony to col- years). When the brown tide in Narragansett Bay was min-
ony, suggesting preferential feeding during the bloom, imal and short-lived in summer 1986, some of these inimical
In November-December 1987 there was an unprecedented effects reversed and there were more cladocerans and bay
episode of human shellfish poisoning due to consumption of anchovy eggs.
mussels (Mytilus edulis) from Prince Edward Island (P.E.I.), There were similar ecosystem disruptions during Long Is-
Canada. This resulted in three human deaths and 107 cases land brown tides in 1985 and 1986 (Cosper et al. 1987).
of gastrointestinal illness and amnesic shellfish poisoning Although most of the zooplankton of Great South Bay on
(ASP), or permanent short-term memory loss (Per1 et al. the south shore of Long Island did not exhibit reduced abun-
1990; Todd 1993). The agent for the ASP was the neurotox- dances during the 1985 bloom compared to the reduced 1986
in, domoic acid (DA), produced by the diatom Pseudo- bloom, abundances of summer bivalve larvae were an order
nitzschia multiseries (Bates et al. 1989) which had been in- of magnitude higher in 1986 than in 1985 (Duguay et al.
gested by the mussels. This was the first report of shellfish 1989). This suggests that bay scallop recruitment failures in
toxicity due to a diatom. Subsequently there have been 1985 (Bricelj et al. 1987) may have been due to starvation
DA-producing blooms at PE.1. in 1988 (Smith et al. 1990) of planktonic larvae (Gallagher et al. 1989).
and in other locations around North America (Villac et al. There are several indications that the brown tide blooms
1993). Among these was an outbreak of DA toxicity in Mon- were largely ungrazed by metazoans. Durbin and Durbin
terey Bay, California, where anchovies, having fed on a (I 989) found that when the copepod A. tonsa collected from
bloom of Pseudo-nitzschia australis, were vectors for lethal brown tide water were fed the palatable diatom Thalassiosira
seabird intoxication (Fritz et al. 1992; Work et al. 1993). DA weissflogii they had higher feeding and egg production rates
from undigested cells in the anchovy guts points to a short than on a diet of brown tide algae. These measurements in-
food chain between the source of the toxin and fish-eating dicated that copepods were severely food limited in Narra-
birds. However, the most likely pelagic consumers of dia- gansett Bay during the brown tide and starvation may have
toms such as Pseudo-nitzschia would be zooplankters such been the major cause of plankton decreases during the 1985
as copepods. blooms.
Windust (1992) examined the potential of DA to inhibit Since 1990 a brown tide has also frequented portions of
grazing by copepods and for copepods to transport DA to the south Texas coast (Buskey and Stockwell 1993; Stock-
higher trophic levels. Although dissolved DA had dose-de- well et al. 1993; Whitledge 1993). As noted for the north-
pendcnt toxicity for the copepods Temora Zongicornis and eastern U.S. brown tides, there have also been substantial
Pseudocalanus acuspes at concentrations in the mg ml-’ declines in populations of mesozooplankton, dominated by
range, these concentrations were over three orders of mag- the copepod A. tonsa (Buskey and Stockwell 1993). Reduc-
nitude higher than maximum DA levels measured during the tions in A. tonsa body size, gut pigment content, and egg
1988 PE.1. bloom. There was no toxic effect at similar high production during the brown tide suggest that this alga was
levels on the larger copepod Calanus glacialis. To test poorly grazed. The cause of the unpalatability of brown tide
whether ingested DA had more profound effects than ex- algae is not clear, but Tracey et al. (1988) suggested that an
posure to dissolved DA, Windust performed several exper- external layer of polysaccharidelike material covering the
iments comparing feeding responses of copepods to toxic P. cell may interfere with motion of mussel gill cilia, either by
multiseries and nontoxic P. pungens. There were no differ- clogging or chemical irritants or toxicants.
ences in feeding rates of C. glacialis and T. Zongicornis on Phaeocystis is an important bloom-forming genus in tem-
toxic and nontoxic forms and no apparent effects of DA on perate and polar seas (Davidson and Marchant 1992). The
copepod gut-filling rates, feeding behavior, or survival. Co- life cycle of Phaeocystis includes solitary flagellated cells
pepods were capable of both uptake and retention of ingested 3-8 p,rn in diameter, as well as colonial aggregations of hun-
DA because DA was detected after gut evacuation. This find- dreds of nonflagellated cells embedded in gelatinous matri-
ing suggests that copepods may act as mechanisms for vec- ces of up to 2-mm diameter (Rousseau et al. 1994).
torial transport of DA to zooplanktivorous consumers, al- Gelatinous Phaeocystis colonies can form enormous nui-
though no cases of higher trophic level impacts have been sance blooms contributing to anoxia, beach fouling, and
reported. clogging of bivalve gills and fishing nets (Lancelot et al.
In summers 1985 and 1986 there were unprecedented 1987, WeiBe et al. 1994). Phaeocystis may also be toxic in
blooms of a previously undescribed picoplanktonic (2-3 that the antibiotic acrylic acid (Sieburth 1960) or dimethyl-
pm) chrysophyte A. anophageflerens (Sieburth et al. 1988) sulfide (Liss et al. 1994) may be either contained in or ex-
at several locations along the northeastern coast of the US, creted from colonies,
(Cosper et al. 1989; Smayda and Villareal 1989a). The 1985 The gelatinous and(or) possibly toxic nature of this alga
brown tide in Narragansett Bay had deleterious effects on has led to what Huntley et al. (1987b) called the “legend of
zooplankton and other organisms at several trophic levels Phaeocystis unpalatibility to zooplankton” (see Tande and
(see Smayda and Fofonoff 1989; Smayda and Villareal Bamstedt 1987; WeiBe et al. 1994). This possibility is sup-
1989b). Included were reduced abundances of the dominant ported by numerous observations of reduced abundances of
metazoan zooplankters such as the copepod A. tonsa, de- zooplankton associated with Phaeocystis blooms (Davies et
pression of the normal summer marine cladoceran commu- al. 1992; Turner 1994). There are numerous indications from
nity (Evadne nordmani and Podon spp.) to mean abundances field and laboratory studies that blooms of colonial Phaeo-
1208 Turner and Tester

cystis are not extensively grazed by or are even deleterious toxic A. tamarense, as well as numerous other phytoplankton
to copepods (Schnack et al. 1985; Verity and Smayda 1989). and diatom species known to be nontoxic. Thus, rotifers like
During a spring bloom in the English Channel, Bautista et other grazers, exhibit varied responses when feeding on var-
al. (1992) found that there were lower levels of copepod gut ious toxic phytoplankters and results of such interactions are
fluorescence, ingestion rates, and copepod abundance during highly specific for particular combinations of predators and
a period of Phaeocystis abundance than during a previous prey *
period of diatom dominance. Combining individual copepod
ingestion rates with copepod abundances allowed Bautista et Accumulation, transport, and effects of phycotoxins
al. to conclude that community grazing impact was minimal
in pelagic food webs
during the bloom, mainly due to anomalously low copepod
abundances (Davies et al. I992).
Reduced grazing on Phaeocystis could also be due to poor Grazers function as vectors for transport of phycotoxins
nutritional value. During a bloom in the Irish Sea, Phaeo- to zooplanktor, predators such as fish. Most information on
cystis had a low content of polyunsaturated fatty acids and this subject comes from the seminal work on paralytic shell-
vitamin C; comparison of the biochemical composition of fish poisoning (PSP) toxins from A. tamarense in the Bay
copepod fecal pellets and Phaeocystis revealed that cope- of Fundy (Whl te 1977, 1979, 1980, 1981a).
pods fed primarily on diatoms rather than Phaeocystis during During a fish kill accompanying an A. tamarense bloom
the bloom (Claustre et al. 1990). in July, 1976, stomachs of dead adult Atlantic herring (Clu-
pea harengus narengus) contained algal remains, pteropods
(Limacina retroversa), and PSP toxins. Comparable levels
interactions of toxic phytoplankters with of PSP toxins ..n adult herring resulted in immediate abnor-
microzooplanktonic grazers mal swimming behavior, paralysis within tens of minutes,
and death withj n 2 h. White (I 977) concluded that PSP tox-
Protists-Interactions between toxic phytoplankton and ins had been ingested by eating pteropods which had grazed
microzooplankton have been less-studied than those with co- on A. tamaren&e.
pepods and results are mixed. Although some tintinnids se- During a blos3m in 1977, PSP toxins were found in plank-
lectively prey upon toxic and nontoxic dinoflagellates, other ton samples obtained with net meshes of 20, 64, 243, and
dinoflagellates are poor food (Stoecker et al. 1981). Exudates 571 pm. Maximum toxin content was in the >20-pm frac-
of A. tamarense and Alexandrium ostenfeldii cause reversals tion, dominated by A. tamarense; progressively lower toxin
of ciliary motion in some tintinnids with abnormal contin- levels were found in net fractions dominated by tintinnids
uous backwards swimming or death (Hansen 1989; Hansen with ingested A. tamarense (>64 pm), marine cladocerans,
et al. 1992). Also several tintinnid species exhibit reduced and small copepods (>243 km) and larger copepods (>57 I
growth and survival on diets of toxic dinoflagellates such as km). Because there were no dinoflagellates or tintinnids in
Gyrodinium aureolum (Hansen 1995) or other toxic Aagel- the larger net fractions, White (1979) concluded that these
lates that are not dinoflagellates such as H. carterae and C. larger zooplankters had accumulated toxins through inges-
polylepis (Verity and Stoecker 1982; Carlsson et al. 1990). tion. Levels of PSP toxin in these larger fractions were high-
Heterotrophic dinoflagellate species may consume other er than those shown to be lethal to small adult herring, sug-
toxic bloom-formers. Several laboratory studies suggest that gesting that dense blooms of A. tamarense could cause
predation of heterotrophic dinoflagellates on autotrophic di- substantial mortality of fish by ingestion of PSP-containing
noflagellates could be an important regulator of red tide zooplankton.
bloom development and decline (Jeong and Latz 1994; Nak- In subsequenl kills of adult herring during A. tamarense
amura et al. 1992, 1995; Burkholder and Glasgow 1995). blooms, dying fish were observed swimming abnormally and
Also some tintinnids and heterotrophic dinoflagellates can gulping for breal:h, and stomachs of dead fish contained algal
ingest free-swimming solitary Phaeocystis cells or pick sol- residue, PSP toxins, and were packed with marine cladoc-
itary cells off of gelatinous colonies (Admiraal and Vene- erans (E. nordmani) which also contained A. tamarense re-
kamp 1986; WciBe and Scheffel-M&er 1990). mains. Zooplankton samples dominated by E. nordmani also
contained toxins. PSP toxins were present only in fish vis-
Rotifers-Solne toxic algae are ingested by rotifers with cera and were absent from muscle tissue, indicating that tox-
varying effects. Mallin et al. (1995) found that feeding on ins ingested through zooplankton vectors quickly kill fish.
the toxic dinoflagellate Pfiesteria piscicida caused no appar- White (1980) concluded that there was strong circumstantial
ent deleterious effects in terms of reduced fecundity or in- evidence that fish kills during toxic algal blooms were from
creased mortality on the rotifer Brachionus plicatilis, but this fish eating intoxified zooplankton such as the pteropods in
rotifer exhibited reduced feeding compared to nontoxic algae the 1976 bloom or the cladocerans during the 1979 bloom.
on H. carterae (Chotiyaputta and Hirayama 1978) and Texas He noted that in a 1968 sand lance kill during a Gonyaulax
brown tide (Buskey and Hyatt 1995). H. carterae was also bloom in British waters (Adams et al. 1968), that E. nord-
not ingested by the marine rotifer Synchaeta Cecilia (Egloff mani had also bl:en a dominant zooplankter, and ingestion
3986) and this alga inhibited feeding on other acceptable of toxin-contaminated zooplankton had also been suggested
phytoplankters at abundances as low as 50 cells ml- I and (but not demonstrated) to be the cause of the fish kill.
reduced rotifer survival and reproduction at levels > 10X I Oj White (1981a,r used laboratory experiments to confirm
cells ml- I. Egloff (1988) found that S. Cecilia did not eat that A. hudsoniw and barnacle nauplii could ingest toxic A.
Toxic algae and grazers 1209

tamarense and accumulate toxins with no apparent adverse move > 100% of the A. tamarense population daily. Popu-
effects. Toxins were retained in the organisms for several lations of A. tamarense and polychaete larvae crashed within
days after gut evacuation, suggesting incorporation into so- days of each other, the latter crash likely caused by larval
matic tissues. Turriff et al. (1995) and Teegarden and Cem- settlement. Whether such a process translocates toxins from
bella (1996) subsequently confirmed that Alexandrium spp. the plankton to the benthos is unknown. During the same
toxins accumulate in several other species of copepods (C. blooms, Watras et al. (1985) measured both dinoflagellate
jinmarchicus, A. tonsa, E. herdmani) and Boyer et al. (1985) growth rates and zooplankton community grazing rates with
found that Protogonyaulax catenella toxin accumulates in radioactive tracers and concluded that loss of A. tamarense
the copepod Tigriopus californicus. to grazers could play a significant role in regulating timing
Additional studies have confirmed that dinoflagellate tox- and magnitude of blooms in these embayments because
ins are lethal to larvae, juveniles, or adults of several species community grazing rates often exceeded rates of dinoflagel-
of fish. Intoxication can be by direct exposure to toxin, in- late population growth.
gestion of toxic dinoflagellates, or ingestion of zooplankton Uye (1986) estimated copepod community grazing impact
that had ingested dinoflagellates (White 1981b; White et al. on development of C. antiqua blooms in the Seto Inland Sea
1989; Mills and Klein-Macphee 1979; Gosselin et al. 1989; of Japan. At minimum field concentrations (20 cells ml-l),
Huntley 1989; Riley et al. 1989; Robineau et al. 19916; Niel- copepod communities could daily graze 3.4-30.8% of the
sen 1993). C. antiqua population. Grazing pressure decreased with in-
Robineau et al. (199lb) compared feeding by larvae of creasing C. anfiqua abundance, with only 1.8% of the C.
the Atlantic mackerel (Scomber scorn&us) and the lobster antiqua population removed at maximum field abundance
(Homarus americanus) on toxic A. excavatum, and adult co- levels. Uye concluded that copepod grazing pressure could
pepods that had eaten toxic A. excavatum. Lobster larvae be important in retarding the initial stages of bloom devel-
were apparently unaffected, but poisoned fish larvae exhib- opment when both water temperature and concentrations of
ited the same symptoms of erratic swimming, sinking, and C. antiqua were low. However, under conditions favorable
immobility prior to death recorded for other studies. These for flagellate growth, copepod grazing pressure would be
results, combined with those from cited studies on fish, adult vastly exceeded by C. antiqua growth, so that at peak abun-
crabs, crab larvae, bivalves, euphausiids, copepods, and lob- dance levels (>500 cells ml-‘), the bloom would be virtually
sters led Robineau et al. (199 la) to suggest that invertebrates immune to grazing impact.
can generally accumulate PSP toxins without lethal effects, Sellner and Olson (1985) also found minimal losses to
whereas nervous systems of fish, humans, and other verte- copepod grazing during dinoflagellate blooms in Chesapeake
brates are far more susceptible to lethal inhibition of axonal Bay and its embayments-generally <5% of field dinofla-
conduction by sodium channel blocking. gellate populations per day for E. afinis grazing on H. tri-
First-feeding larvae of various fish species ingest dino- quetra, and A. tonsa feeding on Katodinium rotundatum and
flagellates or herbivorous zooplankton (Turner 1984), so Gymnodinium nelsoni. Sellner et al. (199 1) found that daily
phycotoxins could potentially cause significant mortality on grazing impact by rotifers, copepods, and copepod nauplii
emerging year-classes of fish if their critical period for larval on a winter bloom of K. rotundatum in the Patuxent River
feeding and survival (Hjort 1914; Lasker 1971) coincided estuary of Chesapeake Bay increased from 13% of dinofla-
with blooms of toxic dinoflagellates. Many later stage larvae gellate biomass in December to 67% during the peak bloom
and postlarvae, although primarily zooplanktivorous and less and copepod abundance period in February. Sellner et al.
susceptible to direct intoxication, still might be at risk of (199 1) concluded that grazing could remove substantial por-
vectorial intoxication. tions 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
Impact of zooplankton grazing on development and
losses (Sellner and Brownlee 1990).
persistence of harmful algal blooms There is considerable evidence that the northeastern U.S.
and Texas brown tide blooms may have been triggered by
Impacts of zooplankton community grazing pressure on breakdowns in grazing at several trophic levels. Although
development and termination of toxic phytoplankton blooms picoplankters the size of A. anophag&erens can be eaten by
arc variable and outcomes appear situation-specific. During filter-feeding bivalves (Tracey 1988), most grazing on these
spring blooms of A. tamarense in Cape Cod embayments in small cells would be presumed from heterotrophic protists.
1980, Turner and Anderson (1983) measured rates of rc- Mesozooplanktonic suspension-feeders such as copepods are
moval of A. tamarense by copepods and planktonic poly- thought to be unable to efficiently graze on picoplankters,
chaete larvae from mixtures of natural seawater spiked with but copepods are known to prey on the heterotrophic protists
A. tamarense cultures. Because of low individual grazing that eat picoplankters (Turner and Roff 1993). Thus, the rel-
rates due to cold temperatures and low abundances of co- ative levels of predation by copepods on heterotrophic pro-
pepods, copcpod community grazing impact on A. tamarense tists, and of these protists on brown tide picoplankters, may
populations was minimal, with a maximum removal of only be important factors in bloom development.
1% d -I. This was not the case, however, for polychaete lar- Caron et al. (1989) examined consumption of brown tide
vae because they were very abundant (855 liter- I). Even organisms by planktonic protists and estimated the effects of
with lower individual grazing rates than copepods it was this picoplankter on microprotistan grazing in Long Island
estimated that the population of polychaete larvae could re- embayments. Brown tide algae supported rapid growth of
1210 Turner and Tester

some heterotrophic protists but allowed only slow growth or plankton abundance and grazing rates before and after brown
no growth of others. Addition of A. anophagefirens to nat- tide development support the conclusion that the Texas
ural water promoted increases in abundance of protists and brown tide bloom was largely uncontrolled by grazing (Bus-
decreases in the brown tide alga, suggesting grazing by pro- key and Stockwell 1993).
tists. Estimates of predation on fluorescently labeled algae
or bacteria by natural assemblages of protists in Long Island Conclusions
waters affected by brown tide revealed no reduction of pro-
tistan grazing during brown tide blooms. Together these ob- An overall synthesis of interactions between toxic phy-
servations suggest that protistan grazing should keep levels toplankton and their grazers is elusive because blooms and
of brown tide algae reduced to the point of retarding bloom grazer interactions are situation-specific. Many contradic-
development but that a critical factor may be the abundance tions are due to a variety of toxins which may have different
of potential protistan consumers of brown tide algae at the physiological effects on consumers and to differences in tox-
time of bloom initiation, because once a bloom becomes in potency or intracellular concentrations due to genetic vari-
established, it appears capable of explosively outgrowing ability, uncontrolled culture conditions, or environmental
protistan predation. Caron et al. speculated that heavy pre- variations that are not accounted for in natural blooms. Dif-
dation by larger zooplankters on the protistan predators of ferent grazers also exhibit different responses to different
brown tide algae may provide ephemeral windows of op- toxic phytoplankton species or to different clones or blooms
portunity for successful initiation of brown tide blooms. of the same spl=cies. Additional complications can arise from
Smayda and Villareal (1989b) concluded that the 1985 effects of organisms at other trophic levels that, while not
brown tide in Narragansett Bay may also have been triggered direct grazers of toxic phytoplankton, may affect their
during a period of reduced grazing. They proposed that dur- blooms by preying on their grazers. Accordingly, informa-
ing the late spring-early summer transition from winter- tion from one experimental study or natural bloom is diffi-
spring bloom to summer conditions there is an open niche cult to extrapolate to another.
in the phytoplankton of Narragansett Bay and that compe- Despite this complexity, it is clear that improved under-
tition for and occupancy of this niche can be determined by standing of to.uic phytoplankton blooms will emerge with
complex trophic interactions. In some cases the toxic fla- more effort to define the role of zooplankton grazers. Both
gellate H. carterae wins the competition by allelochemic in- zooplankton population monitoring and studies of zooplank-
hibition of the frequently dominant, rapidly growing diatom ton grazing and food-web interactions should be incorporat-
S. costatum (Pratt 1966). In other cases, S. costatum blooms ed into phytoplankton monitoring programs focused on
in summer because ctenophore predation on copepods re- harmful blooms. In the very few cases where ongoing phy-
duces copepod grazing pressure on diatoms (Deason and toplankton and zooplankton monitoring preceded develop-
Smayda 1982) or H. carterae blooms because its toxicity ment of a harmful bloom (e.g. Buskey and Stockwell 1993;
inhibits copepod grazing (Tomas and Deason 1981). Buskey and Hyatt 1995), the impact of zooplankton grazing,
Smayda and Villareal (19896) suggested that the 1985 and or its absence, seemed important in bloom dynamics.
1986 brown tides may have been differentially regulated by We recommend that studies of toxic phytoplankton, graz-
heterotrophic flagellate grazing. During the latter half of ers, and food-web interactions be conducted with more at-
summer 1985 abundance of brown tide algae declined while tention to variations in intracellular toxin concentrations and
phagotrophic flagellate abundance increased. The implica- potency. Also, grazing studies should extend beyond unial-
tion is that the flagellates grazed down the brown tide until gal cultures to include ingestion of naturally co-occurring
its disappearance in October 1985. Brown tide reappeared in nontoxic as well as toxic phytoplankters in natural assem-
high abundance (up to 254X 10” cells liter-‘) in mid-May blages. Through collaboration between phytoplanktologists,
1986, persisting through June when it co-occurred with a zooplanktologists, and phycotoxin chemists a better under-
bloom of H. carterae and minimal levels of S. costatum. standing of interactions between toxic phytoplankton, their
This was the reverse of the 1985 situation when S. costatum grazers, and marine food webs will emerge.
was abundant and H. carterae was not. However, the most
substantial difference in early summer 1986 was high abun- References
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