Comparative analysis of three brevetoxin-associated bottlenose dolphin (Tursiops truncatus) mortality events in the Florida Panhandle region (USA).

Michael J Twiner,Sabrina R Bowen-Stevens,Spencer E Fire,Blair Mase-Guthrie,Zhihong Wang,Joseph K Gaydos,Teresa K Rowles,Christine K Johnson,Jan H Landsberg,Tod A Leighfield,Lori Schwacke,Frances M Van Dolah,Leanne J Flewelling

doi:10.1371/journal.pone.0042974

Abstract

In the Florida Panhandle region, bottlenose dolphins (Tursiops truncatus) have been highly susceptible to large-scale unusual mortality events (UMEs) that may have been the result of exposure to blooms of the dinoflagellate Karenia brevis and its neurotoxin, brevetoxin (PbTx). Between 1999 and 2006, three bottlenose dolphin UMEs occurred in the Florida Panhandle region. The primary objective of this study was to determine if these mortality events were due to brevetoxicosis. Analysis of over 850 samples from 105 bottlenose dolphins and associated prey items were analyzed for algal toxins and have provided details on tissue distribution, pathways of trophic transfer, and spatial-temporal trends for each mortality event. In 1999/2000, 152 dolphins died following extensive K. brevis blooms and brevetoxin was detected in 52% of animals tested at concentrations up to 500 ng/g. In 2004, 105 bottlenose dolphins died in the absence of an identifiable K. brevis bloom; however, 100% of the tested animals were positive for brevetoxin at concentrations up to 29,126 ng/mL. Dolphin stomach contents frequently consisted of brevetoxin-contaminated menhaden. In addition, another potentially toxigenic algal species, Pseudo-nitzschia, was present and low levels of the neurotoxin domoic acid (DA) were detected in nearly all tested animals (89%). In 2005/2006, 90 bottlenose dolphins died that were initially coincident with high densities of K. brevis. Most (93%) of the tested animals were positive for brevetoxin at concentrations up to 2,724 ng/mL. No DA was detected in these animals despite the presence of an intense DA-producing Pseudo-nitzschia bloom. In contrast to the absence or very low levels of brevetoxins measured in live dolphins, and those stranding in the absence of a K. brevis bloom, these data, taken together with the absence of any other obvious pathology, provide strong evidence that brevetoxin was the causative agent involved in these bottlenose dolphin mortality events.

Highlights

Harmful algal blooms (HABs) are commonly known for their detrimental impacts on aquatic organisms, human health, and local economies [1,2,3]
Human health effects from brevetoxins generally result from neurotoxic shellfish poisoning (NSP) [11] and/or respiratory illness caused by inhalation of aerosolized toxin [12]
K. brevis and Pseudo-nitzschia spp. cell counts reported here were obtained from FWC-FWRI’s Harmful Algal Bloom database, which contains statewide HAB data collected for monitoring, research, and event response

Summary

Introduction

Harmful algal blooms (HABs) are commonly known for their detrimental impacts on aquatic organisms (including marine mammals), human health, and local economies [1,2,3]. Often referred to as ‘‘Florida red tide’’, occur in the Gulf of Mexico (Florida, USA) on a nearly annual basis [4] This dinoflagellate produces a suite of neurotoxins known as brevetoxins (PbTxs or BTXs), which are heat-stable, lipid-soluble, polyether compounds [5,6,7]. Human health effects from brevetoxins generally result from neurotoxic shellfish poisoning (NSP) [11] and/or respiratory illness caused by inhalation of aerosolized toxin [12]. The former can occur following consumption of contaminated shellfish that have accumulated sufficient levels of toxin while filter feeding the algal assemblage including K. brevis. NSP typically affects the nervous and gastrointestinal systems; all symptoms are reversible and to date there have been no human associated deaths [3,11]

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