Cyanobacteria and prawn farming in northern New South Wales, Australia—a case study on cyanobacteria diversity and hepatotoxin bioaccumulation

Abstract

Harmful cyanobacteria pose a hazard to aquatic ecosystems due to toxins (hepatotoxic microcystins, nodularins, and cylindrospermopsin) they produce. The microcystins and nodularins are potent toxins, which are also tumor promoters. The microcystins and nodularins may accumulate into aquatic organisms and be transferred to higher trophic levels, and eventually affect vector animals and consumers. Prawn farming is a rapidly growing industry in Australia. Because information regarding effects of cyanobacteria at prawn farms was lacking, we examined diversity of cyanobacteria and toxin production plus bioaccumulation into black tiger prawns ( Penaeus monodon) under both field (northern New South Wales, Australia, December 2001–April 2002) and laboratory conditions. Samples were analyzed for hepatotoxins using enzyme-linked immunosorbent assay (ELISA) and high-performance liquid chromatography (HPLC). The maximum density of cyanobacteria (1 × 10 6 to 4 × 10 6 cells/l) was reached in April. Cyanobacteria encountered were Oscillatoria sp. (up to 4 × 10 6 cells/l), Pseudanabaena sp. (up to 1.8 × 10 6 cells/l), Microcystis sp. (up to 3.5 × 10 4 cells/l), and Aphanocapsa sp. (up to 2 × 10 4 cells/l). An uncommon cyanobacterium, Romeria sp. (up to 2.2 × 10 6 cells/l), was also observed. Contrasting earlier indications, toxic Nodularia spumigena was absent. Despite that both Oscillatoria sp. and Microcystis sp. are potentially hepatotoxic, hepatotoxin levels in phytoplankton samples remained low (up to 0.5–1.2 mg/kg dw; ELISA) in 2001–2002. ELISA was found suitable not only for phytoplankton but prawn tissues as well. Enzymatic pretreatment improved extractability of hepatotoxin from cyanobacteria (nodularin from N. spumigena as an example), but did not generally increase toxin recovery from prawn hepatopancreas. There were slightly increasing hepatotoxin concentrations in prawn hepatopancreas (from 6–20 to 20–80 μg/kg dw; ELISA) during the study. Hepatotoxin concentrations in surface sediment remained low (<5 μg/kg dw; ELISA) throughout the study. Laboratory experiments indicated that prawn hepatopancreas, heart, and brain were primary organs for hepatotoxin bioaccumulation. Toxin concentration in other organs, including muscle, was less effective. Orally administered nodularin levels in hepatopancreas rapidly decreased from initial 830 to 250 μg/kg dw in 96 h. Similarly, concentration of microcystin-LR injected in prawns decreased from 130 to 30 μg/kg dw (hepatopancreas) in 2 h. These results demonstrate that potential risks caused by cyanobacteria in prawn farming (farmers, prawns, and consumers) were not substantial in 2001–2002. Although prawns may act as vectors for toxin transfer, they did not accumulate alerting amounts of hepatotoxins and were able to effectively detoxify them. Because bloom toxicity may vary, low-frequency toxin monitoring is recommended.