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 Articles and gems - Harmful algal blooms in marine wildlife populations
Abstract
 Natural toxins from marine algae blooms - like synthetic pesticides - can cause
mortality in wildlife populations. A variety of wildlife types are affected because of
trophic transport and bioaccumulation in the pelagic food web. Detecting phycotoxins at
concentrations low enough to allow detection in field populations of zooplankton - the primary
entry point to the food web - has been the biggest obstacle to the study of vectorial
intoxication of higher organisms.
As analytical techniques improve, algal toxins can be
detected, identified, and monitored more accurately. This may be particularly important if
harmful algal blooms are increasing in frequency or expanding their range. Effects of
algal toxins on marine wildlife should prove to be similar to those of toxicants already
known to negatively affect wildlife populations.
Introduction
The effects of environmental contaminants on wildlife usually bring to mind images of
Rachel Carson and her timely warnings about the wholesale destruction of wildlife from
the spraying of pesticides. Others perhaps think of PCBs in the Great Lakes and envision
birds with malformed bills and reproductive failure.
No matter the scenario, synthetic
chemicals, or toxicants, are most often associated with negative effects on wildlife
populations and the habitats they occupy. Yet even before the pesticides that alarmed
Ms. Carson became widely available, toxins produced by harmful algal blooms (HABs;
often referred to as "red tide") were responsible for mortality events involving
piscivorous birds.
For instance, in 1942 McKernan and Scheffer reported mortality of common murres
(Uria aalge) and loons (Gavia spp.) from an outbreak off the coast of
Washington state (Nisbet, 1983). Die-offs caused by lethal algae blooms continued to be
reported in the United States and in other parts of the world throughout the 1950s, 1960s,
and 1970s, often affecting large numbers of breeding birds such as cormorants
(Phalacrocorax spp.), northern fulmars (Fulmarus glacialis), herring gulls
(Larus argentatus), and terns (Sterna spp.) (Nisbet, 1983;
http://www.marinelab.sarasota.fl.us).
HABs are frequent along the coasts of Canada and Mexico as well as the United States. In fact,
in 1996, red tides were the most frequent cause of environmental emergencies affecting the
marine ecosystem in Mexico (Table 1) (Ochoa et al., 1998). Other hotspots occur in waters
off South America, the North Sea coast of the United Kingdom, and the shores of Scandinavia,
Hong Kong, and Japan (Anderson, 1994; Nisbet, 1983; Ochoa, 1998;
http://www.marinelab.sarasota.fl.us).
Once a concern only for human health, HABs have increasingly been implicated by researchers
in marine wildlife die-offs. Many times the researchers’ conclusion came as a surprise both
to the public, saddened by massive wildlife deaths, and to the scientists themselves working
to discover why the animals died. Not unexpectedly, pollution was often blamed initially for
unusual mortality events, and toxicant assays traditionally have been one of the first steps
in finding an answer to them.
Now, fortunately, marine wildlife experts are quicker to
recognize that algal toxins may be responsible when die-offs occur. Questions still loom,
however, about the ecology of toxic algae and how toxins are transported to animals higher in
the pelagic food web. As these questions are answered, and as techniques for analyzing and
monitoring phycotoxins improve, the impact of HABs on wildlife populations will become clearer.
A history of bloom-related wildlife die-offs
The Monomoy National Wildlife Refuge in Massachusetts was the scene of an HAB mortality
event in 1978. More than 70 birds from a breeding colony of common terns
(S. hirundo), arctic terns (S. paradisaea), and roseate terns (S. dougallii)
, as well as herring gulls and laughing gulls (L. atricilla), died after ingesting the
same toxin that
causes paralytic shellfish poisoning (PSP) in humans. The PSP toxin was in the birds’
primary food source, the sand lance (Ammodytes americanus), in levels lethal to birds
(Nisbet, 1983).
Mortalities are not limited to birds. During November of 1987 wildlife along the Massachusetts
coast were again affected by the PSP saxitotoxin. Fourteen dead humpback whales
(Megaptera novaeangliae) washed ashore along the beaches of Cape Cod Bay and Nantucket
Sound. The deaths of even small numbers of charismatic megafauna often get media attention,
and this event was no exception
While it is not uncommon for toothed whales to strand in groups, humpbacks are baleen whales,
which strand only rarely and usually singly. With fourteen dead humpbacks in five weeks,
the press and the public blamed a chemical spill or other pollution. As it turned out, however,
the whales had eaten Atlantic mackerel (Scomber scombrus) whose organs tested
positive for the PSP toxin (Anderson and White, 1992; Geraci et al., 1989).
At the same time – June 1987 to February 1988 – more than 740 bottlenose dolphins
(Tursiops truncatus) were found dead along the Atlantic coast from New Jersey
to Florida. Levels of PCBs and DDT were high in some of the animals, but many others
tested in the same range as aquarium dolphins. Because the whale deaths had been traced
successfully to a red tide toxin, a similar approach was used in this case.
The geographic range of the saxitoxin that killed the whales was too far north for the
same organism to be implicated, but a different alga which produces a suite of toxins
known as brevetoxins is prevalent along the west coast of Florida. As it turned out,
brevetoxins, the cause of neurotoxic shellfish poisoning (NSP) in humans, were transported
via the Gulf Stream to the North and South Carolina coasts where they were responsible
for a major red tide in October 1987.
Several cases of NSP and respiratory problems and
eye irritation among fishermen and beachgoers led the public initially to suspect that
a nearby sunken submarine was leaking poison gas. Dolphins migrating through this area
could certainly have been exposed to the toxin as well, but there is only speculation
about the dolphin deaths from June to October. A red tide in
the Gulf of Mexico from January to April 1987 is believed to have traveled south and
around the tip of Florida
to the Atlantic Ocean. Menhaden (Brevoortia tyrannus), which are filter feeders,
and Spanish mackerel (S. maculatus), which are menhaden predators, are abundant
in these waters. Dolphins eat both of these fish (Anderson, 1994; Anderson and White, 1992).
The first fish kill in Florida suspected to have been caused by red tide was in 1844.
Since that time harmful algal blooms have been reported every few years killing fish,
seabirds, and marine mammals, often in large numbers. In 1957, catastrophic mortality was
reported for marine mammals from Anclote Key to Cape Sable. Thirty-nine endangered Florida
manatees (Trichechus manatus) were also lost to brevetoxins in 1982 and more
than 150 were lost in 1996. Both stomach contents and lung tissue contained the toxin,
indicating that the toxins entered through the food web as well as from direct contact
with aerosols at the water’s surface
(http://www.marinelab.sarasota.fl.us and
http://www.whoi.edu/info/red-tide.html).
The northern California coast is another story, however. When a sudden mass mortality of
brown pelicans (Pelecanus occidentalis) and Brandt’s cormorants
(P. penicillatus) occurred near Santa Cruz in 1991, wildlife authorities were puzzled.
Assays for pollutants, including pesticides and heavy metals, provided no answers.
On the chance that algal toxins were involved, mouse bioassays – the standard test for PSP –
were conducted on both the birds stomach contents and the northern anchovies
(Engraulis mordax) on which they had been feeding. The injected mice started
scratching behind their ears, reminding the veterinarian in charge of an article in
which the test mice exhibited similar symptoms.
In that case study four years earlier,
more than 100 people in eastern Canada fell ill to a new type of poisoning now referred
to as amnesiac shellfish poisoning (ASP) resulting from a new algal toxin called domoic
acid. When pelican and anchovy stomach contents were sent to the same Canadian researchers,
high levels of domoic acid were found in both. Later tests revealed that domoic acid was
present not only in the viscera, but also in the flesh of the fish, leading to the closure
of the anchovy fishery (Anderson, 1994; Anderson and White, 1992; Work et al., 1993).
Note
The original article contains sections on bloom dynamics at this point.
Why do algae produce toxins?
Considerable study has yet to provide a satisfactory answer. Phycotoxins seem to have evolved,
at least in part, as a defense mechanism against zooplankton and other grazers,
but since nontoxic algae also form blooms it is unlikely that this is their sole function.
The search for biochemical pathways within the algae that require the toxins has yielded
little information. Phycotoxins are not proteins and are synthesized in a series of
chemical steps that require multiple genes.
So far, no chemical intermediates or
enzymes used only in toxin production have been isolated. Clues about toxin metabolism
have been somewhat more promising, indicating that it is a dynamic process. Certain
strains of dinoflagellates produce different amounts of toxin and different toxin
derivatives when growth conditions are varied in the laboratory. Still,
without the identification of a specific biochemical role, it may be that
accidental chemical affinity of phycotoxin metabolites for receptors on the
ion channels of other animals may be responsible for the mass mortalities
higher in the food web (Anderson, 1994).
Bacteria living in the dinoflagellate cell may also play a role in the production
of phycotoxins. Intracellular bacteria isolated from antibiotic-treated algal
cultures have produced saxitoxin in very small quantities. Synergism between bacteria
and the host cell has been indicated, or alternatively, bacterial genes or plasmids
may be involved (Anderson, 1994).
Three genera of phytoplankton account for most of the harmful algal blooms in U.S. waters:
- Alexandrium spp. and Karenia spp. are dinoflagellates;
- Pseudonitzschia spp. are diatoms.
Note
The original article contains more information about these three genera and their toxins
as well as a section on monitoring. (Picture on the right is Trichodesmium spp. - from NOAA.)
Are harmful algal blooms increasing?
Advances in technology are also at the center of a debate concerning the scale of
HABs worldwide. Maps point to an expansion of HAB events in the US since 1972,
but provide no information about the frequency of events or whether the spread is the
result of natural processes or human activities. On one side of the controversy are
those who assert that HABs are natural phenomena and serve a purpose in the ecology of
the coastal systems in which they occur
(http://www.marinelab.sarasota.fl.us).
What appears to be an expansion of events is simply the result of heightened awareness
of HABs because of increased aquaculture, greater communication among scientists,
and better detection methods (Ochoa, 1997).
There is certainly support for this point of view. The 1987 K. breve outbreak
along the Carolina coast was a natural occurrence with no link to human activities.
A Florida bloom was carried north by the Gulf Stream, a theory since supported by
satellite images of sea surface temperatures from that period. Similarly, it was a
1972 hurricane that introduced A. tamarense cysts into southern New England waters,
where the organism still persists. Finally, better chemical instrumentation has
enabled researchers to identify new toxins from species formerly considered nontoxic
(Anderson, 1994;
http://www.whoi.edu/info/red-tide.html).
On the other side, arguments can be made for a trend toward HABs growing worse over
the last few decades. A variety of factors including human activity support this position.
In addition to dispersal by currents and storms, phytoplankton cysts can be spread by
shellfish seeding and by bilge water from transglobal ships. More than 300 million
dinoflagellate cysts were found in the ballast tank of a single ship (Anderson, 1994).
Changing climate conditions could also play a part in increasing the frequency of
toxic blooms. For instance, colder water conditions in the Gulf of California in
recent years, due in part to upwelling from strong northwest winds, may promote conditions
such as increased levels of carbon dioxide that are ideal for dinoflagellate blooms, but
limit diatoms, most of which are harmless (Ochoa et al., 1998).
More importantly, the link between pollution and HABs should not be ignored. Long-term
studies at the local and regional level show that red tides are increasing as the
eutrophication of coastal waters from industrial, agricultural, and domestic waste increases.
For example, when the population around Tolo Harbor in Hong Kong grew sixfold between
1976 and 1986, red tides increased eightfold. Red tides in the Inland Sea of Japan rose
from 44 per year in 1965 to more than 300 in 1975. Strongly enforced effluent controls
begun in the mid-1970s resulted in a 50 % reduction in toxic events (Anderson, 1994).
As much as both examples could be criticized as cases of heightened awareness or
better detection, an obvious relationship should exist between excess nutrients
in the water and a general increase in algal growth. All phytoplankton should benefit,
but some scientists have used the nutrient ratio hypothesis to suggest that pollution
selectively stimulates the growth of toxic species. For example, diatoms require silicon
in their cell walls while other phytoplankton, including dinoflagellates, do not. Silicon
is not abundant in sewage, but nitrogen and phosphorus are, resulting in an increase in
nitrogen to silicon and phosphorus to silicon ratios in coastal waters in recent years.
When silicon supplies are depleted, diatom growth stops but other, often toxic, algae
proliferate using the excess nitrogen and phosphorus (Anderson, 1994).
Note
The original article contains a more extensive discussion.
Conclusions
Simply looking at changes in the pattern of occurrence of HABs doesn’t paint the entire
picture. At first glance the obvious is true, more blooms create the possibility of more
die-offs; but the long-term impact may be more insidious. Studies of pesticides and birds
of prey have shown two types of effect on wildlife populations – an increase in
mortality rates and a decrease in population growth rates (Walker, 2001). There is no
reason to think that the effects of natural chemicals on wildlife populations are any
different.
Whether HABs are expanding their range and increasing in frequency or whether they
are simply being detected and reported more accurately, there is no doubt that mass
mortalities in animals at the top of the pelagic food web can be attributed to phycotoxins.
A lack of documentation of HABs as the cause of death until the past few decades may simply
be due to inadequate knowledge of the ecology of toxic phytoplankton.
As these events are studied more carefully and as technology improves methods for the
detection, identification, and analysis of algal toxins, fewer mortality events are likely
to be shrouded in mystery or written off to general pollution. An accurate assessment of
the effects of harmful algal blooms on wildlife populations will allow wildlife
experts to treat dangers from natural toxins in the same way that they treat
dangers from synthetic chemicals.
References:
- Anderson, D.M. 1994. Red tides. Sci. Amer. Aug:62-68.
-
Anderson, D.M. 1997. Diversity of harmful algal blooms in coastal waters.
Limnol. Oceanogr. 42(5):1009-1022.
-
Anderson, D.M., and A.W. White. Marine biotoxins at the top of the food chain.
Oceanus 35(3):55-61.
-
Geraci, J.R., D.M. Anderson, R.J. Timperi, D.J. St Aubin, G.A. Early, J.H. Prescott, and C.A.
Mayo. 1989. Humpback whales (Megaptera novaeangliae) fatally poisoned by
dinoflagellate toxin. Can. J. Fish Aquat. Sci. 46:1895-1898.
- Mote Marine Laboratory web site (accessed 11-27-01).
Red tide update, phytoplankton ecology. Sarasota, Florida.
-
Nisbet, I.C.T. 1983. Paralytic shellfish poisoning: effects on breeding terns.
Condor 85:338-345.
-
NYSDEC web site (New York State Department of Environmental Conservation)
(accessed 12-11-01). Cormorant studies and management in New York. Division of Fish,
Wildlife, and Marine Resources.
-
Ochoa, J.L., A. Sanchez-Paz, A. Cruz-Villacorta, E. Nunez-Vazquez, and A. Sierra-Beltran.
1997. Toxic events in the northwest Pacific coastline of Mexico during 1992-1995:
origin and impact. Hydrobiologica 352:195-200.
-
Ochoa, J.L., A.P. Sierra-Beltran, G. Olaiz-Fernandez, and L.M. Del Villar-Ponce.
1998. Should mollusk toxicity in Mexico be considered a public health issue?
J. Shellfish Res. 17(5):1671-1673.
-
Turner, J.T., G. J. Doucette, C.L. Powell, D.M. Kuris, B.A. Keafer, and D.M. Anderson. 2000.
Accumulation of red tide toxins in larger size fractions of zooplankton assemblages
from Massachusetts Bay, USA. Mar. Ecol. Prog. Ser. 203:95-107.
-
USFDA web site
(United States Food and Drug Administration) (accessed 11-27-01).
Foodborne pathogenic microorganisms and natural toxins handbook.
USFDA, Center for Food Safety and Applied Nutrition.
-
Walker, C.H., S.P. Hopkin, R.M. Sibly, and D.B. Peakall. 2001. Principles of
Ecotoxicology. Taylor and Francis, London.
-
WHOI web site (Woods Hole Oceanographic
Institution) (http://www.redtide.whoi.edu, accessed 11/27/01). The harmful algae page. Woods Hole, Massachusetts.
Now at http://www.whoi.edu/info/red-tide.html.
-
Work, T.M., A.M. Beale, L. Fritz, M.A. Quilliam, M. Silver, K. Buck, and J.L.C. Wright. 1993.
Domoic acid intoxication of brown pelicans and cormorants in Santa Cruz, California.
In Toxic Phytoplankton Blooms in the Sea, T. J. Smayda and Y. Shimizu, eds., Elsevier
Science Publishers B.V., Amsterdam, 643-649.
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