Abstract:
The 2017–2019 harmful algal bloom in southwest Florida resulted in the largest number of sea turtle deaths ever attributed to a single red tide event. The mass mortality of sea turtles associated with this event clearly demonstrates the impacts of brevetoxicosis, but there is an urgent need to characterize the sublethal, chronic effects of brevetoxins on wildlife. Marine turtles can be exposed to brevetoxins through inhalation of aerosolized toxins, but the most lethal route of exposure is through ingestion of prey items that contain accumulated brevetoxins. Sea turtles are notoriously resilient and able to withstand severe physical damage but they appear to be surprisingly susceptible to biological and chemical insults.
Many studies document the acute impacts of brevetoxicosis in stranded and rehabilitated turtles showing obvious clinical symptoms, but few characterize the chronic effects of brevetoxins on wildlife health. This study evaluates the sublethal effects of red tide blooms on nesting loggerhead sea turtles and their hatchlings.
Between 2019 and 2022, we collected 428 blood samples from 305 nesting loggerheads without clinical evidence of brevetoxicosis. We also collected 276 dead-in-nest hatchlings and 1,593 eggs from nests laid by these females. Plasma, hatchling livers, and egg contents were analyzed for total brevetoxins. Hatching success was used as an index for reproductive output. Maternal plasma brevetoxin concentrations were low in comparison to animals that strand during red tide blooms, ranging from 0.1 to 24.6 ng/mL Stable isotope analysis indicated that loggerheads foraging in the Gulf of Mexico had significantly higher plasma brevetoxin concentrations than those using Caribbean foraging grounds. Several correlations of brevetoxins with blood analytes provided evidence of subclinical effects on immune functions and overall health. Mean hatchling liver brevetoxin concentrations ranged from 12.0 to 534.0 ng/g and were significantly higher in 2020 and 2021 compared to 2019. Brevetoxin concentrations in hatchling livers and eggs from the same nest were significantly correlated, but no correlations were observed between these values and maternal brevetoxin concentrations. Hatching success did not significantly correlate with plasma, egg, or liver brevetoxin concentrations. Histopathologic evaluation of hatchling tissues was performed, but indicated no relationship with brevetoxin concentrations in hatchling livers. Our results provide evidence that even when harmful algal blooms do not cause direct mortality of exposed wildlife, they can potentially act as a physiological stressor with long-term impacts on the health of sea turtles. Additionally, our data confirm that toxin transfer occurs from nesting female to egg/offspring, with high values reported in many hatchling liver tissues, but brevetoxins do not appear to impact reproductive success. The combination of global climate change, potential tropical cyclone intensification, and eutrophication will likely increase the incidence and intensity of harmful algal blooms. It is important to consider the impacts of these blooms on sea turtle health and reproduction when evaluating stressors on the population and developing management strategies.
Suggested Citation:
Andrew Glinsky, Jack Brzoza, Nicole I. Stacy, Paul Julian, Simona A. Ceriani, Susan Fogelson, Justin R Perrault. Characterizing the relationships between brevetoxin concentrations, blood analytes and reproductive success in nesting loggerhead sea turtles (Caretta caretta) and their offspring in southwest Florida, USA (2019 - 2021). Distributed by: GRIIDC, Harte Research Institute, Texas A&M University–Corpus Christi. doi:10.7266/7h818h5z
Purpose:
Our purpose was to investigate the long-term effects of a red tide event on the health and reproductive success of nesting loggerhead sea turtles (Caretta caretta). This was achieved by (1) quantifying brevetoxin concentrations in plasma for loggerheads nesting on Sanibel Island, Florida, USA, following an intense and prolonged red tide bloom, (2) establishing correlations with brevetoxin exposure and blood analytes, (3) determining brevetoxin concentrations in unhatched egg contents and dead-in-nest hatchling livers, and (4) identifying impacts of brevetoxin exposure on hatching success.
Data Parameters and Units:
Date, location Turtle ID, Turtle length (cm), hatch success (%), washovers, sample number, maternal PbTx-3 (ng/g), mean egg PbTx-3 (ng/g), mean hatchling liver PbTx-3 (ng/g), d13Cepi, d15Nepi, QDA, packed cell volume (l/l), Total solids (g/dl), Hemolysis, Albumin (g/dL), Amylase (u/L), Calcium (mg/dL), Chloride (mmol/l), Cholesterol (mg/dL), Glucose (mg/dl), Lipase (u/L), Phosphorus(mg/dL), Potassium (mmol/l), Sodium (mmol/l), BUN (md/dL), Uric Acid (mg/dl), Triglycerides (mg/dl), Protein total (g/dl), CPK (U/L), AST (U/L), GGT (U/L), alpha globlin(g/dl), beta globulin (g/dl), gamma globulin (g/dl), A:G (g/dl), White Blood Cell estimate (K/ul), Heterophils (/ul), Immature heterophils (K/ul), Lymphocytes (K/ul), Monocytes (K/ul), Eosinophils (K/ul), Basophils (K/ul), Heterophils:Lymophocytes
Methods:
Sanibel Island (26.4648°N, -81.1671°W) is a coastal barrier island located on the southwest coast of Florida, U.S.A. The island is 21 km in length with a land area of 4,429 ha and hosts an average of 612 ± 55 loggerhead nests annually. Inconel flipper tags and a PIT tag were applied to nesting loggerhead females and morphometric data were taken. Skin and scute biopsies were taken for stable isotope analysis for each turtle. 10 mL of whole blood was collected from the external jugular vein and kept on ice in the field until centrifugation within 1–9 hours. At inventory, up to 3 unhatched eggs and dead-in-nest hatchlings were collected from each clutch for brevetoxin analysis. One lobe of the liver was removed from each hatchling.
To analyze the maternal health, blood smears were used to analyze complete blood counts with differentials (heterophils, lymphocytes, monocytes, eosinophils, basophils) and observations of red (RBC) and white blood cell (WBC) morphology. Packed cell volume (PCV) was determined using whole blood. A full biochemistry panel was completed for all plasma samples. Protein electrophoresis was carried out to determine pre-albumin, albumin, alpha-, beta-, and gamma-globulin fractions.
For brevetoxin analysis, plasma was analyzed for brevetoxins using an indirect competitive enzyme-linked immunosorbent assay (ELISA) following manufacturer’s instructions (MARBIONC, Wilmington, NC, USA; Naar et al., 2002). Brevetoxins in unhatched eggs and livers from dead-in-nest hatchlings were extracted with methanol or acetone, defatted with hexane, and passed through a 0.45 µm filter before using the ELISA assay. For hatchling pathology -- Whole, formalin-fixed bodies from 55 dead-in-nest loggerhead hatchlings were submitted to Fishhead Labs, LLC (Stuart, FL, USA) for gross examination, processing, and subsequent histological evaluation.