Biomagnification or biodilution of microcystins in aquatic foodwebs? Meta-analyses of laboratory and field studies

Cyanobacteria, conspicuous photoprokaryotes in aquatic ecosystems, may produce secondary metabolites such as the hepatotoxins, microcystins (MC). While MC have been quantified in numerous aquatic consumers across a variety of ecosystems, there is still debate whether biomagnification or biodilution of MC generally occurs in aquatic foodwebs. Given the threat that MC pose to aquatic foodwebs, livestock, and humans, we synthesized data from 42 studies on the concentration of MC in consumers, such as zooplankton, decapods, molluscs, fishes, turtles and birds, to determine the dominant process. To compare results across studies, we calculated the biomagnification factor (BMF) as the ratio between the MC concentration measured in consumers and their diet. Biomagnification is indicated when BMF mean and associated 95% confidence intervals (CI) >1. Biodilution is shown if a BMF mean and 95% CI <1. As expected, increasing concentrations of MC in diets resulted in increasing concentrations of MC in consumers. Nevertheless, biodilution of MC was evident for most primary consumers. This finding was robust across four datasets that focused on different aspects of data independence and variance, and may be explained by low hydrophobicity of MC, diet preferences, or detoxification. Zooplankton and zooplanktivorous fish, however, showed some potential for biomagnification (i.e. mean BMF > 1). Plausible, but largely unexplored, possibilities for the relatively higher MC accumulation by these consumers are low detoxification efficiency by zooplankton, MC trophic transfer via the microbial foodweb, contamination of zooplankton net samples with large cyanobacterial colonies and filaments, or the release of both free and bound MC in zooplankton during digestion by fish. Factors related to study design may have influenced the magnitude of MC biodilution. For example, consumers fed diets consisting of highly toxic cyanobacterial lab cultures and large, potentially inedible net phytoplankton showed greater biodilution when compared to seston. Given their hepatotoxic nature, MC concentrations were relatively higher in liver and hepatopancreas tissues than other tissues. Whole organisms exhibited, however, relatively greater MC (i.e. higher BMF) than specific tissues, and this finding could be attributed to the contribution of zooplankton to whole organism MC analyses (89% of BMF estimates > 1). Finally, BMF was positively related to study length showing that longer exposure to toxic food resulted in higher MC accumulation in consumers, which could have important implications in eutrophic or tropical systems where toxic blooms may persist year-round. 2012 Elsevier B.V. All rights reserved. * Corresponding author. Tel.: +1 334 246 1120; fax: +1 334 844 9208. E-mail addresses: [email protected] (B. Kozlowsky-Suzuki), [email protected] (A.E. Wilson), [email protected] (A.S. Ferrão-Filho).