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Paralytic shellfish toxins in southern rock lobster : physiological impact and improving public health risk management

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Turnbull, AR ORCID: 0000-0001-5701-8728 2021 , 'Paralytic shellfish toxins in southern rock lobster : physiological impact and improving public health risk management', PhD thesis, University of Tasmania.

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Abstract

During 2012 an extensive bloom of the toxic dinoflagellate Alexandrium catenella occurred on the east coast of Tasmania causing paralytic shellfish toxins (PST) to accumulate in bivalve shellfish at 12 times the regulatory maximum level (ML; 0.8 mg STX.2HCl equiv. kg\(^{−1}\)). Southern Rock Lobster, Jasus edwarsdii, accumulated PST in the hepatopancreas to 3.9 mg STX.2HCl equiv. kg\(^{−1}\), resulting in the first closure of an Australian lobster fishery due to marine biotoxins. Recurrent blooms since 2012 have had an on-going impact on both the commercial fishery in Tasmania, valued at AUD 93 M, and the significant recreational fishing sector.
The present body of work aimed to address the following knowledge gaps exposed by this novel risk: (1) the toxicokinetics associated with PST uptake and depuration in J. edwardsii from A. catenella blooms; (2) the impact of PST on lobster health; (3) the supply chain risk of PST accumulation in J. edwarsdii; and (4) to determine and validate where appropriate cost-effective methods to appropriately monitor and manage PST accumulation in lobster the field.
In elucidating these questions, information was sought that could inform management of public health and market access risks and determine whether PST accumulation could adversely affect lobster performance, health and catchability.
To examine toxicokinetics of PST in J. edwardsii (Aim 1), an experimental study was undertaken in a biosecure aquaculture facility in South Australia. Adult male lobsters were fed highly toxic mussels (6 mg STX.2HCl equiv. kg\(^{−1}\)) sourced from the impacted area in Tasmania for four weeks, then allowed to depurate for a further 5 weeks. Control (fed non-toxic mussels) and exposed lobster were harvested at regular intervals, tissues dissected and analysed for PST. The lobsters rapidly accumulated PST in the hepatopancreas (exponential rate of 6% per day), exceeding the bivalve ML within one week, and reaching a maximum of 9.0 mg STX.2HCl equiv. kg\(^{−1}\). Once toxic feed was removed, the lobster depurated at a rate of 7% per day. Toxins were found in lobster antennal glands at concentrations two orders of magnitude lower than found in the hepatopancreas. This is the first report of PST in lobster antennal glands which, along with the gills, represent possible excretion routes for PST. However, PST were not detected at significant levels in the lobster haemolymph, which means there is no option for non-destructive sampling of lobster for PST.
During the experiment, lobster health was assessed to determine the impact of PST accumulation in the hepatopancreas (Aim 2). A comprehensive range of behavioural (vitality score, righting ability and reflex impairment score), health (haemocyte count, bacteriology, gill necrosis and parasite load), nutritional (hepatopancreas index and haemolymph refractive index) and haemolymph biochemical (21 parameters including electrolytes, metabolites, and enzymes) parameters were examined. Accumulation of PST increased the apparent feed intake but did not result in mortality nor significant changes in the behavioural, health, or nutritional measures suggesting limited gross impact on lobster performance. Furthermore, most haemolymph biochemical parameters measured exhibited no significant difference between control and exposed animals. However, in the lobsters fed toxic mussels, the concentration of potassium in the haemolymph increased with PST, whilst the concentration of lactate and the sodium:potassium ratio decreased with PST. In addition, lobsters with elevated levels of PST in the hepatopancreas showed a hyperglycaemic response, indicative of stress. These findings suggest that PST accumulation results in some measurable indicators of stress for lobsters, but these changes appear to be within the adaptive range for J. edwardsii and do not result in a significant impairment of gross performance.
To determine whether J. edwardsii could accumulate PST in the supply chain (Aim 3), a controlled experiment was conducted where adult male lobsters were exposed to highly toxic cultures of A. catenella at field relevant concentrations (2 × 10\(^5\) cells L\(^{−1}\)) over a period of 21 days. In contrast to the feeding experiment, no PST accumulated in lobster from exposure to toxic algal cells. The same lobster health parameters were assessed, with no change seen in any of the behavioural, health, nutritional or haemolymph biochemical parameters examined.
To assess appropriate management strategies (Aim 4), regulatory monitoring results since September 2012 were combined with field studies to examine uptake and depuration of toxins in J. edwardsii on the east coast of Tasmania during A. catenella blooms. Results from 496 lobster hepatopancreas PST samples were analysed. A high degree of variability was seen across years, months, sites and between individuals. The highest risk sites are on the central east coast, with exceedances of the bivalve ML occurring between July and January. Mussel sentinel lines were installed in each lobster management zone on the east coast of Tasmania and monitored fortnightly during high-risk periods. These lines proved effective in indicating a risk of elevated PST in lobster hepatopancreas. Field uptake and depuration rates of PST in lobster were similar to those seen during the experimental studies (maximum of 2% and 3% per day respectively), but always less than rates measured simultaneously in mussels. Analysis of hepatopancreas PST levels during bloom development and decline occurred to determine the level of confidence in the regulatory sampling regime (5 individual lobster hepatopancreas samples are analysed from each site during an event). When PST in the hepatopancreas of all lobsters sampled is < 0.5 mg STX.2HCl equiv. kg\(^{−1}\) there is 97.5% confidence that any lobster from that site would be below the bivalve ML.
In conducting this research, it became apparent that international regulations for maximum levels of PST in seafood and research into PST accumulation vary in the units used for PST concentration. Some standards/research reports use mg STX.2HCl equiv. kg\(^{−1}\), some mg STX equiv. kg\(^{−1}\) (effectively producing total PST results that are 24% lower), and some only state mg kg\(^{−1}\). Similarly, the toxic equivalency factors (TEF) used to convert analogue concentrations to total PST in toxicity equivalents are varied, and often not stated. A call for uniform reporting units was published in Toxicon correspondence to highlight this issue, recommending countries and researchers adopt the Codex Alimentarius Commission protocols of reporting in mg STX.2HCl equiv. kg\(^{−1}\), using FAO/WHO TEF.
The combined field and experimental work detailed in this thesis has informed improvements to the biotoxin risk management program for J. edwardsii in Tasmania. Implications for biotoxin risk monitoring are: (1) lobsters continue to feed during bloom periods and high concentrations of PST can occur; (2) animal toxin monitoring should be frequent at the start of a bloom in case of a rapid accumulation of PST; (3) mussel sentinel lines are a cost-effective early warning system for toxin accumulation; (4) it is adequate to sample 5 individuals per site as long as a reduced trigger level of closure of harvest is employed; (5) depuration is relatively quick at up to 7% per day so that sampling to confirm re-opening should occur soon after bloom collapse (as indicated by mussel PST levels); (6) non-lethal sampling is not possible as haemolymph PST levels do not reflect levels in the hepatopancreas. Importantly, (7) lobsters exposed to toxic algae during wet storage in long supply chains (on vessel, in sea-cages or at processing facilities) do not take up PST. Furthermore, (8) survival, quality, and safety of this high-value product are not impacted by accumulation of PST or by exposure to toxic cells in the water.

Item Type: Thesis - PhD
Authors/Creators:Turnbull, AR
Keywords: Marine biotoxins, toxic algae, Alexandrium, lobster, risk management, toxicokinetics, stress response.
Copyright Information:

Copyright 2021 the author

Additional Information:

Chapter 2 appears to be the equivalent of a post-print version of an article published as: Turnbull, A., Malhi, N., Seger, A., Harwood, T., Jolley, J., Fitzgibbon, Q., Hallegraeff, G., 2020. Paralytic shellfish toxin uptake, tissue distribution, and depuration in the Southern Rock Lobster Jasus edwardsii Hutton, Harmful algae 95, 101818.

Chapter 3 appears to be the equivalent of a post-print version of an article published as: Turnbull, A., Malhi, N., Seger, A., Jolley, J., Hallegraeff, G., Fitzgibbon, Q., 2021. Accumulation of paralytic shellfish toxins by Southern Rock lobster Jasus edwardsii causes minimal impact on lobster health, Aquatic toxicology, 230, 105704.

Chapter 4 appears to be the equivalent of a post-print version of an article published as: Turnbull, A., Seger, A., Jolley, J., Hallegraeff, G., Knowles, G., Fitzgibbon, Q., 2021. Lobster supply chains are not at risk from paralytic shellfish toxin accumulation during wet storage, Toxins, 13(2), 129. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/).

Chapter 5 appears to be the equivalent of a post-print version of an article published as: Turnbull, A., Dorantes-Aranda, J. J., Madigan, T., Jolley, J., Revill, H., Harwood, T., Hallegraeff, G., 2021. Field validation of the southern rock lobster paralytic shellfish toxin monitoring program in Tasmania, Australia, Marine drugs, 19(9), 510. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/).

Chapter 6 appears to be the equivalent of a post-print version of an article published as: Turnbull, A. R., Harwood, D. T., Boundy, M. J., Holland, P. T., Hallegraeff, G., Malhi, N., Quilliam, M. A., 2020. Paralytic shellfish toxins - call for uniform reporting units, Toxicon 178, 59-60.

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