Abstract
Exposure of common bottlenose dolphins (Tursiops truncatus) to brevetoxins (PbTx) produced by blooms of the toxic phytoplanktonKarenia brevisfrequently results in severe health impacts, including illness and large-scale mortality events. Although PbTx accumulation in dead-stranded dolphins is well documented, there are limited data for corresponding brevetoxin exposure in live dolphins. In addition, the severity of impacts on living survivors of such toxic blooms is difficult to assess due to a lack of data on the relationship betweenK. brevisbloom severity and corresponding PbTx concentrations in exposed animals. Here we present results of PbTx analysis of urine, serum, milk, gastric fluid, and feces samples collected from live, free-ranging dolphins (n= 253) from Sarasota Bay, Florida during 2000–2018, and investigate the relationship between PbTx concentrations detected and correspondingK. breviscell abundances that are temporally (within 30 days) and spatially (within 16 km) associated with each individual. We found that 28% of dolphins were associated with elevatedK. brevisabundances (10,000–60,000,000 cells/L), with 41% (n= 104) of dolphins testing positive for PbTx in at least one sample type. The proportion of PbTx-positive animals was significantly greater in animals exposed to elevated cell abundances vs. those exposed to background cell abundances (<10,000 cells/L), with 60 and 34% testing positive, respectively (p< 0.001). PbTx was detected most frequently in feces (57%,n= 38), followed by gastric (35%,n= 37), urine (32%,n= 55), and blood (7%,n= 17). PbTx concentrations by sample type were highest in feces (2–231 ng/g; mean 46), followed by urine (0.8–90 ng/g; mean 7.2), gastric (0.8–61 ng/g; mean 12), and blood (0.3–5 ng/g; mean 1.3). Regression analyses ofK. breviscell abundance as an index of exposure vs. corresponding PbTx concentration found no statistically significant relationship for feces (p= 0.120), gastric (p= 0.349), urine (p= 0.053), or blood (p= 0.729) samples. PbTx concentrations typically ranged over two orders of magnitude between minimum and maximum values and did not scale with corresponding indices of exposure, which ranged over three orders of magnitude or more. Our results indicate thatK. breviscell abundance alone is a poor predictor of brevetoxin accumulation in bottlenose dolphins, and suggest that alternative methods (e.g., endocrine or immunological biomarkers) should be investigated as more appropriate methods for determining the severity of health impacts due to red tides.
Highlights
Harmful algal blooms (HABs) are frequently associated with morbidity and large-scale mortalities of marine mammals, due to exposure to potent neurotoxins produced during such events (Broadwater et al, 2018; NOAA, 2020)
Important marine sentinel species such as the common bottlenose dolphin (Tursiops truncatus) are apex predators that are typically distanced from toxic phytoplankton by several trophic links, with the organisms in each link having distinct rates of toxin accumulation and/or depuration (Landsberg, 2002; Doucette et al, 2006; Naar et al, 2007)
Should a strong correlative relationship exist between the toxin concentration detected in an animal and the severity of the HAB to which it was exposed, this would serve as a useful tool to predict toxin accumulation in individuals or back-calculate toxic phytoplankton abundances associated with mortality events
Summary
Harmful algal blooms (HABs) are frequently associated with morbidity and large-scale mortalities of marine mammals, due to exposure to potent neurotoxins produced during such events (Broadwater et al, 2018; NOAA, 2020). Previous work has suggested that the abundance of toxic phytoplankton alone is a poor predictor of toxin accumulation rates and likelihood of exposure in dead-stranded marine mammals (Fire et al, 2007, 2020a; Landsberg et al, 2009). This is primarily due to the fact that apex predator marine mammals do not graze on phytoplankton nor ingest large amounts of seawater, accumulate negligible amounts of HAB toxins transdermally or via inhalation, leaving dietary intake (through large fish and invertebrates) as the only feasible route of biologically significant exposure. The relationship between phytoplankton abundance and toxin accumulation in exposed animals has not been demonstrated for live, free-ranging marine mammals
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