Because the animal samples were collected for other research projects unrelated to our research on cyanobacteria blooms and the BMAA hypothesis, the spatial and temporal patterns of animal samples are not optimal for examining the hypothesized link between cyanobacteria blooms and BMAA accumulation in animals. Nevertheless, these initial results indicate that high concentrations of BMAA can accumulate in some aquatic animals in areas of cyanobacteria blooms. Not enough samples have been analyzed to discern any clear patterns, but some possibilities do appear.
In south Biscayne Bay, there was large variation in the BMAA concentrations between individuals of a species in pink shrimp, blue crabs, mojarra, band tail puffers, least puffers, and bluestriped grunts (). The replicability of our methods suggest that these differences are real and not the result of methodological problems. The cause of this variation is unknown but several possibilities exist. As these animals were collected from an area north of the bloom, depending on their migration patterns, some animals may have spent considerable time in the bloom (or the organisms in their diet did so) while others may have spent little or no time in the bloom. While our research focussed on planktonic cyanobacteria, benthic cyanobacteria and cyanobacteria epiphytic on seagrass and macroalgal blades are also present. In these shallow waters, microalgal abundance per square meter is typically around 20 times higher on the sediment surface than in the water column above (Brand and Suzuki, 1999
). Microhabitat differences in the relative abundance of these different groups of cyanobacteria and their BMAA content might account for the differences observed. Genetic differences between individuals in their ability to accumulate BMAA are also a possibility (discussed below), just as there are genetic differences among humans in their susceptibility to develop neurodegenerative diseases. Whatever the cause of this variation, it must be kept in mind when examining data on only a few individuals of a species.
Many crustaceans appear to have high concentrations of BMAA. Pink shrimp in Florida Bay () have high concentrations of BMAA, comparable to those found in the fruit bats of Guam (3556 μg/g; Cox et al., 2003
). Pink shrimp and blue crabs in south Biscayne Bay have a wide range of concentrations (). All three species of fish from the Caloosahatchee River () have high concentrations of BMAA similar to that of the fruit bats of Guam. The filter feeding molluscs in the Caloosahatchee River and estuary have only moderate amounts of BMAA (). Grey snapper in Florida Bay south of its cyanobacteria bloom have moderate amounts of BMAA (), while grey snapper in Biscayne Bay north of its cyanobacteria bloom have none ().
In south Biscayne Bay, a wide range of BMAA concentrations was observed among the 17 species examined. A perusal of the data does not reveal a classical biomagnification pattern, as top carnivores such as barracuda and grey snapper show no BMAA, while species near the bottom of the food chain, such as pink shrimp, pufferfish, and sea bream have relatively high concentrations. A pattern that does appear, however, is a tendency for higher concentrations of BMAA in species that feed on the benthos, and lower concentrations in species that feed on the plankton. An exception to this pattern is pinfish, which primarily feed on benthic vegetation, but had no BMAA. No BMAA was found in anchovies, silversides, needlefish, and barracuda that feed in the water column, while high concentrations were found in pink shrimp, blue crabs, pufferfish, and cowfish that feed on the bottom. This could be an indication that benthic cyanobacteria produce more BMAA than planktonic species, but we have no direct information on this. A perusal of the data of Cox et al. (2005)
does suggest that such a pattern may exist.
At the present time, we do not know why cyanobacteria produce BMAA and thus, what environmental patterns may exist. Similarly, we do not know the mechanism of bioaccumulation of this amino acid. Because BMAA is water soluble, the standard mechanism for biomagnification of lipophilic compounds is not plausible. One possibility is differential uptake and excretion. Because BMAA is structurally similar to glutamate in the presence of bicarbonate as a carbamate (Weiss et al., 1988
), neutral acid uptake enzymes in the gastrointestinal tract and elsewhere may take up BMAA from dietary sources, but enzymes involved in the turnover, degradation, and excretion of amino acids may not be able to recognize BMAA and eliminate it. A differential in uptake vs. excretion enzymes may be one possible mechanism for the large differences observed between individuals and species in this study.
Ultimately there are many sources of variation that could account for the results shown here. The laboratory data of Cox et al. (2005)
have shown a 500-fold variation in the amount of BMAA produced by cyanobacteria. Much of this is likely the result of genetic differences between species, but some is likely due to physiological differences in response to environmental differences. As a result, one would expect microhabitat variation among benthic and epiphytic cyanobacteria, and differences between planktonic and benthic communities. As BMAA propagates up the food chain, differential uptake and excretion will cause varying amounts of biomagnification. The age of animals could be important, with older animals accumulating more BMAA. The time course of BMAA exposure over the lifetime of an animal could be important, depending on the ability of an animal to slowly or quickly excrete BMAA after short term exposure. While it is clear that most cyanobacteria produce BMAA, we cannot, at this time, be sure that there are no other sources of BMAA such as heterotrophic bacteria.
Based upon this study and other data, it appears that the situation in Guam is not unique, and that high concentrations of BMAA do occur in parts of aquatic food webs. To enhance the chances of finding BMAA in aquatic animals, this study focussed on areas of unnatural blooms of cyanobacteria caused by nutrient enrichment by human activities. Cyanobacteria are of course a significant part of natural aquatic habitats unaffected by human activities. Cyanobacteria are approximately 50% of the phytoplankton community of the open ocean covering over half of the earth (Li et al., 1983
; Itturiaga and Mitchell, 1986
). It is plausible that humans have been exposed to some level of BMAA throughout their evolutionary history. The increase in cyanobacteria blooms as a result of human activities is probably increasing this exposure, but by how much is not yet known. Our research is now expanding from this initial exploratory analysis to determine the distribution of BMAA in aquatic food webs and seafood in both natural ecosystems and eutrophic ecosystems.
Neurodegenerative diseases such as Alzheimer’s disease, Parkinson’s disease, and Amyotrophic Lateral Sclerosis (ALS) are also increasing (Kokmen, et al., 1993
; Gauthier, 1997
; Chio, 2005
). Increased longevity alone may not account for all of this increase. Heritability of these diseases is low, accounting for less that 10% of cases. While certain genetic factors are known to influence susceptibility to these diseases, some unknown environmental factors probably play a major role. BMAA may be a significant environmental factor. Cyanobacteria and the presence of BMAA in portions of aquatic food webs used as human food could be a significant human health hazard.