First report of a toxic Nodularia spumigena (Nostocales/ Cyanobacteria) bloom in sub-tropical Australia. II. Bioaccumulation of nodularin in isolated populations of mullet (Mugilidae)

Abstract

Fish collected after a mass mortality at an artificial lake in south-east Queensland, Australia, were examined for the presence of nodularin as the lake had earlier been affected by a Nodularia bloom. Methanol extracts of muscle, liver, peritoneal and stomach contents were analysed by HPLC and tandem mass spectrometry; histological examination was conducted on livers from captured mullet. Livers of sea mullet (Mugil cephalus) involved in the fish kill contained high concentrations of nodularin (median 43.6 mg/kg, range 40.8-47.8 mg/kg dry weight; n = 3) and the toxin was also present in muscle tissue (median 44.0 μg/kg, range 32.3-56.8 μg/kg dry weight). Livers of fish occupying higher trophic levels accumulated much lower concentrations. Mullet captured from the lake 10 months later were also found to have high hepatic nodularin levels. DNA sequencing of mullet specimens revealed two species inhabiting the study lake: M. cephalus and an unidentified mugilid. The two mullet species appear to differ in their exposure and/or uptake of nodularin, with M. cephalus demonstrating higher tissue concentrations. The feeding ecology of mullet would appear to explain the unusual capacity of these fish to concentrate nodularin in their livers; these findings may have public health implications for mullet fisheries and aquaculture production where toxic cyanobacteria blooms affect source waters. This report incorporates a systematic review of the literature on nodularin measured in edible fish, shellfish and crustaceans.

Keywords: HPLC-MS/MS; Nodularia; cyanobacteria; cyanotoxin; mullet; nodularin; recreational; seafood.

Figure 1

Structure of nodularin.

Figure 2

(a) Reconstructed partial chromatogram of a diluted methanol extract of a sea mullet liver; (b) Reconstructed partial chromatogram of a 100 μg/L nodularin standard solution. Traces shown are for the two transitions monitored, 825.5→135 and 825.5→163. Note the restricted run time (7–11 minutes) plotted on x-axes, employed here to broaden the peaks in order to facilitate visual interpretation.

Figure 3

Mullet livers, fish captured 7 September 2009. Left: Partial liver from study lake specimen. Right: Entire liver from control lake specimen. While the liver of the study lake specimen appeared to be grossly enlarged at necropsy, the two livers presented here are from fish of different size classes, so this image should not be used to draw conclusions on relative liver size.

Figure 4

Removal of mullet liver, study lake capture 7 September 2009. These livers were extremely friable; some broke apart when manipulated. Care was needed in order to remove livers en bloc.

Figure 5

Nodularia trichome fragment from the stomach contents of a sea mullet (Mugil cephalus), study lake fish kill, November 2008.