Surf, bird food, PSP

Toxins along a stirred-up shore

Surf’s up! In early January, high winds stirred the waters of Juneau, making boating an unpleasant if not downright dangerous proposition. The waves pounded the coastlines, roiling the waters next to the shores. Even moderate wave action at the shoreline is sometimes a good thing for hungry birds—the turbulence seems to wash out small invertebrates into open water where ducks can gobble them up, one little item at a time ( It also may loosen cobbles and gravels, making hidden invertebrates accessible to gulls and shorebirds that pick and probe ( Splashes and wetting might encourage upper intertidal mussels relax their tightly closed valves a bit, making it easier for oystercatchers to insert their long, thin bill and extract the soft parts. We see the birds doing these things, but I don’t know that anyone has actually measured the effects of wave action on the inverts…Maybe the birds know more than we do.

Black oystercatcher eating blue mussels. Photo by Bob Armstrong

The oystercatcher feeding on open mussels in the video was filmed in Tee Harbor in spring of 2019, at a time when the level of PSP in the mussels was already high and getting higher. Paralytic Shellfish Poisoning is caused by neurotoxins produced by microscopic algae that feeding molluscs filter from the sea water; certain algal species are especially known for their neurotoxins. The term is earned for the unpleasant and sometimes devastating effects on humans that ingest clams and mussels containing the toxins (and other animals that ate such molluscs). Also, I’ve read that heavy surf can break up the bodies of small planktonic and shoreline organisms, allowing the wind to carry body fragments and neurotoxins as aerosols. By impeding the transmission of nerve impulses, these toxins affect respiration, muscle contraction, and other essential functions. Micro-algae also produce other toxins, which affect digestive systems, memory, and other aspects of consumers.

What about non-human consumers, including the molluscs themselves? Some molluscs just stop feeding when exposed to toxic algae; others are sensitive to the toxins and suffer some negative physiological effects. But some develop resistance to the toxic effects when they are repeatedly exposed to the toxinsand accumulate them in their bodies, in some cases retaining the toxins for many months, passing them on to other consumers. When crabs eat molluscs, they can build up toxins in parts of their bodies too. So sea otters, which eat both molluscs and crabs, may suffer some of the negative consequences; but they can learn to reject prey with high levels of the toxins. Predatory snails (whelks) that feed on mussels and clams ingest the toxins too. And when small fishes (anchovies, sand lance, young salmonids, etc.) and crustaceans feed on the toxic algae in the plankton, and then become prey to other predators, the toxins can pass up the food chain, becoming more concentrated at each step. All around the world, massive die-offs of marine fish (e.g., sardines), mammals (e.g., whales, dolphins, sea lions, seals), and birds (e.g., cormorants, pelicans) have been attributed at least in part to PSP, wreaking havoc in marine communities. 

All those reactions and interactions begin with the neurotoxins in the algae. The toxins are produced all the time by the algae, but the reactions we notice happen more often when there are ‘blooms’ of algae; the blooms result from strong inputs of nutrients (such as nitrogen, iron, and phosphorous) stemming from spring run-off, outflow from melting glaciers, and drifting volcanic ash, which carry minerals dissolved and eroded from rocks and fields. Tides and ocean currents redistribute the nutrients along the coast. Those nutrients allow the algae to reproduce prodigiously, so they are then a super-abundant food source, readily available to consumers.

And that leaves the question of why the algae make those (and several other types of toxins) in the first place. How and why did all those varied compounds arise? So far, I have not found agood answer to that. However, I thought of three kinds of answers: 1) perhaps the compounds contribute to some essential metabolic process or they are produced just as a byproduct in the course of some metabolic, physiological processes that have some effect on growth or reproduction—the toxicity to other organisms is just incidental (from the point of view of the algae).In other words, their function is simply related to the internal workings of the algae. 2) The toxic compounds serve as a defense again would-be consumers, presumably small, planktonic critters (such as copepods) that would feel the direct effects of the toxins and be deterred from eating the algae. There is experimental evidence for this in some cases. In general, the advantage of deterrent or protective effects would be expected in the first level of consumers (the primary consumers); any indirect effects and consequences for secondary consumers higher in the food chain would probably be ‘collateral damage’–irrelevant to algal fitness and the evolution of the compounds. 3) Both #1 and #2 could happen. In other systems, researchers have found that something that arose for one function eventually evolved another function. Given the wide array of micro-algae involved and the variety of compounds that are toxic to many animals, it would not be surprising if all three kinds of answers turn out to be valid. Scientists have a big job ahead of them, to sort out all of this.

A hearty thanks to four fine folks at the NOAA lab who responded so promptly and helpfully to my queries.

PSP and wildlife

how animals deal with one of nature’s potent poisons

Not long ago, I sat on a rock near Auke Rec, watching a squadron of scoters busily diving for mussels. They weren’t doing their coordinated, follow-the-leader diving; each bird was on its own, going down to pull up a mussel.

Photo by Bob Armstrong

That made me recall that spring and summer are usually the times when there are plankton blooms. Along with those events, we usually get reminders about the risks of paralytic shellfish poisoning (PSP). In fact, there was a piece in the Empire some days ago and several warnings on the radio about the unpleasant, sometimes lethal symptoms and noting that cooking does not disable the toxins. Historically, PSP has caused several episodes of multiple human deaths in Alaska.

The tiny organisms in the plankton blooms produce several kinds of toxins. Those that cause PSP are neurotoxic, affecting the nervous system (in multicellular animals that have nervous systems). Nerve impulses require the movement of sodium (and, in some cases, calcium) ions in and out of cells, and the neurotoxins impede that process. So afflicted animals can suffer numbness, paralysis, respiratory failure, and eventually death.

Plankton blooms occur when the water temperature and light are suitable and when nutrient levels are high (which commonly occurs when there is spring runoff from glaciers and freshwater streams). Among the many single-celled organisms that respond in ‘blooms’ are some that are known as dinoflagellates (referring to the whiplike ‘tail’ or flagellum that whirls to propel the cell along). There are hundreds of kinds of dinoflagellates; some are photosynthetic, some are predatory, and some are both.

Many species of dinoflagellates produce toxins of various sorts (in addition to those that induce PSP). Why do they do this? Perhaps as a means of defense against other small organisms that would eat them. Another possibility is that exposure to such toxins in the water might help a predatory dinoflagellate to capture its prey—slowing the prey’s swimming speed, perhaps immobilizing it. So the toxins are always present, but usually at low concentrations—until there is a bloom, and the toxin-producers become very abundant. A recent study showed that a particular dinoflagellate (belonging to the genus Alexandrium, which is said to be the genus most involved in toxic blooms in Alaska) increased its toxin production in response to acidified waters and low phosphorus levels, so that opens the door to potential increases in toxic blooms in the future, as ocean acidification increases (this finding should be verified by additional studies).

After watching those scoters gobbling up mussels, and thinking about the well-advertised effects of PSP on humans, I wondered about the effects of PSP on other, non-human organisms.

When there is a plankton bloom, and toxin-producing organisms are very abundant, all the numerous marine creatures that eat plankton consume vast quantities of the toxins. Many bivalve shellfish (clams, mussels, scallops, etc.) are filter-feeders, sifting plankton from the water, and they can accumulate high concentrations of the toxins. Sometimes the toxins are sequestered in certain parts of the shellfish body, such as the siphon. In some cases, the toxins may be stored for as long as two years (e.g., in butter clams), prolonging the possible effects well beyond the time of the bloom itself.

Do the dinoflagellate toxins poison the invertebrates that eat the dinoflagellates? Potentially, yes. But at least some plankton-eating invertebrates have ways of avoiding serious harm. The softshell clam, for example, develops resistance to the toxin produced by a particular dinoflagellate when it is exposed repeatedly to that toxin. This implies that the biological reason for resistance is that the toxin is damaging; otherwise, why resist? Some plankton-eaters can avoid the toxins by feeding selectively, rejecting potentially toxic dinoflagellates. For example, the Pacific oyster and the northern quahog can simply shut down feeding activity when presented with Alexandrium prey. However, this is not a direct response to the toxins themselves, but rather to the toxin-producer: even non-toxic Alexandrium strains produce the shut-down. In other cases, dinoflagellate toxins can be very damaging to larval invertebrates of several kinds. I find myself wanting to know a lot more about the physiological effects of dinoflagellate toxins on invertebrate consumers and the responses of the consumers to the presence of toxic prey.

Many marine creatures consume the plankton-eaters. Predatory snails that drill into clams or mussels can ingest toxins from the flesh of the prey. Crabs that prey on small molluscs can ingest the toxins too. Zooplankton and small crustaceans, such as krill, consume other plankton and thus become vectors for the toxins. Lots of species of small fishes consume plankton: e.g., sardines, anchovies, sand lance, herring, mackerel, young salmon. Sometimes the level of toxicity is sufficient to kill these fish, and die-offs have been recorded.

Of course, the toxins can move on up the food-chain, when the fish-eaters consume fish that have eaten toxic organisms. When the fish-eaters swallow the whole body of the prey, they obviously get the toxins even if the toxins happen to be only in the digestive tracts of the prey and not throughout the body. The concentrations of toxins tend to increase, as they move up the food-chain. There are numerous records of massive die-offs in North American waters of fish-eating marine birds (terns, gulls, pelicans, scoters, cormorants, murres, loons, etc.), and no doubt many unrecorded incidents of nonlethal illness. Marine mammals can be seriously affected too, including sea lions and humpback whales. Interestingly, sea otters are reported to able to detect the presence of PSP toxins and discard to most toxic parts, or at least just not eat so much. Butter clams are a favorite food of sea otters in some areas, and there the otters can just reject the siphon and other parts where the toxins are concentrated.