Concurrent Exposure of Bottlenose Dolphins (Tursiops truncatus) to Multiple Algal Toxins in Sarasota Bay, Florida, USA

Michael J Twiner,Lori Schwacke,Randall S Wells,Leigh Davidson,Stephen Roth,Brian Balmer,Spencer Fire,Teresa K Rowles,Steve Morton,Zhihong Wang

doi:10.1371/journal.pone.0017394

Abstract

Sentinel species such as bottlenose dolphins (Tursiops truncatus) can be impacted by large-scale mortality events due to exposure to marine algal toxins. In the Sarasota Bay region (Gulf of Mexico, Florida, USA), the bottlenose dolphin population is frequently exposed to harmful algal blooms (HABs) of Karenia brevis and the neurotoxic brevetoxins (PbTx; BTX) produced by this dinoflagellate. Live dolphins sampled during capture-release health assessments performed in this region tested positive for two HAB toxins; brevetoxin and domoic acid (DA). Over a ten-year study period (2000–2009) we have determined that bottlenose dolphins are exposed to brevetoxin and/or DA on a nearly annual basis (i.e., DA: 2004, 2005, 2006, 2008, 2009; brevetoxin: 2000, 2004, 2005, 2008, 2009) with 36% of all animals testing positive for brevetoxin (n = 118) and 53% positive for DA (n = 83) with several individuals (14%) testing positive for both neurotoxins in at least one tissue/fluid. To date there have been no previously published reports of DA in southwestern Florida marine mammals, however the May 2008 health assessment coincided with a Pseudo-nitzschia pseudodelicatissima bloom that was the likely source of DA observed in seawater and live dolphin samples. Concurrently, both DA and brevetoxin were observed in common prey fish. Although no Pseudo-nitzschia bloom was identified the following year, DA was identified in seawater, fish, sediment, snails, and dolphins. DA concentrations in feces were positively correlated with hematologic parameters including an increase in total white blood cell (p = 0.001) and eosinophil (p<0.001) counts. Our findings demonstrate that dolphins within Sarasota Bay are commonly exposed to two algal toxins, and provide the impetus to further explore the potential long-term impacts on bottlenose dolphin health.

Highlights

Harmful algal blooms (HABs) are commonly known for their detrimental impacts on aquatic organisms, human health, and local economies
Human health effects of brevetoxins generally result from neurotoxic shellfish poisoning (NSP) [8] and/or respiratory illness caused by inhalation of aerosolized toxin [9]
Dolphin health assessments corresponded to periods in the bay when K. brevis cell counts were greater than 105 cells/L (Feb 2004, Feb 2005, June 2005), whereas the remaining four health assessments occurred during periods when K. brevis was below the detection limit (June 2000, June 2004, June 2006, May 2008, May 2009)

Summary

Introduction

Harmful algal blooms (HABs) are commonly known for their detrimental impacts on aquatic organisms (including marine mammals), human health, and local economies. Often referred to as ‘‘Florida red tide’’, occur in the Gulf of Mexico (Florida, USA) on a nearly annual basis [1] This dinoflagellate produces a suite of neurotoxins known as brevetoxins (PbTxs or BTXs), which are heat-stable, lipid-soluble, polyether compounds [2,3,4]. Human health effects of brevetoxins generally result from neurotoxic shellfish poisoning (NSP) [8] and/or respiratory illness caused by inhalation of aerosolized toxin [9]. 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. A comprehensive understanding of brevetoxin trophic transfer is lacking, it is clear that finfish [16,17,18] and certain types of seagrasses (i.e., Thalassia testudinum) can accumulate or be associated with brevetoxins and play a primary role in brevetoxin-induced marine mammal Unusual Mortality Events (UMEs) [18,19]

Objectives

Methods

Results

Conclusion