Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs

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