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Mercury and selenium concentrations in stranded bottlenose dolphins from the Indian River Lagoon system, Florida
Abstract and Figures
Mercury is a toxic metallic element that is known to bioaccumulate in many marine organisms. Mercury concentrations are routinely evaluated in Indian River Lagoon (IRL) fish, however, there are no published reports of these concentrations for IRL bottlenose dolphins, Tursiops truncatus (Montagu, 1821). Muscle (n = 30) and liver (n = 19) samples from stranded IRL dolphins were collected and analyzed for total mercury and selenium. Total mercury concentrations in liver samples ranged from 0.42 to 240 ppm wet weight (ww) (mean = 73.01 ppm) and concentrations in muscle samples ranged from 0.26 to 47 ppm ww (mean = 5.68 ppm). Mercury concentrations were not significantly different between males and females for both tissue types. Selenium concentrations ranged from 1.20 to 90.70 ppm ww (mean = 29.81 ppm) in liver tissue and 0.75 to 16.10 ppm ww (mean = 1.92 ppm) in muscle tissue. Selenium concentrations were positively correlated with mercury in both tissue types. Age and total length were good predictors for mercury concentrations in both tissue types. Future studies are needed to determine what effect mercury may have on the overall health of IRL dolphins.
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... The mercury and selenium tissue concentrations in the bottlenose dolphins from this study are within the ranges of those reported for other cetaceans [6,9,18,41,42]. For example, García-Alvarez et al. [43] reported similar mercury (223.8 mg/kg dw) and selenium (68.63 mg/kg dw) concentrations in the liver tissue of bottlenose dolphins from near the Canary Islands to those reported in the present study. Durden et al. [9] reported mean mercury and selenium concentrations of 5.68 (0.26-47) mg/kg ww and 1.92 (0.75-16.1) mg/kg ww in the muscle and 73.0 mg/kg ww (0.42-240) and 29.8 (1.20-90.7) ...
... For example, García-Alvarez et al. [43] reported similar mercury (223.8 mg/kg dw) and selenium (68.63 mg/kg dw) concentrations in the liver tissue of bottlenose dolphins from near the Canary Islands to those reported in the present study. Durden et al. [9] reported mean mercury and selenium concentrations of 5.68 (0.26-47) mg/kg ww and 1.92 (0.75-16.1) mg/kg ww in the muscle and 73.0 mg/kg ww (0.42-240) and 29.8 (1.20-90.7) mg/kg ww in the liver of stranded bottlenose dolphins from the Indian River Lagoon, FL. ...
... Durden et al. [9] reported a positive correlation between tissue (muscle and liver) mercury concentrations and the age of bottlenose dolphins, like other studies [43,47]. In the present study, we found significant differences in the mercury concentration in the muscle and liver between age classes, with a positive effect of age class on the mercury concentration in the muscle. ...
Bottlenose dolphins (Tursiops truncatus) are long-lived marine mammals, upper-level predators, and they inhabit near-shore environments, which increases their exposure to pollution. Mercury is a ubiquitous and persistent metal pollutant that can bioaccumulate and biomagnify up the food chain. Dolphins are known to accumulate mercury, and limited research has shown that mercury exposure can weaken the immune system of dolphins. The objectives of this study were to assess the mercury concentrations in the tissues (muscle, small intestine, liver) of stranded bottlenose dolphins and to compare the tissue mercury levels in dolphins that were stranded during the 2013–2015 morbillivirus Unusual Mortality Event (UME; immunosuppressed individuals) with the levels of those that were stranded at a normal rate (2016–2021). Selenium has been shown to reduce mercury toxicity in many animals; therefore, tissue selenium concentration and the molar ratio of selenium to mercury were also assessed. The tissue mercury (muscle, liver) and selenium (liver) concentrations increased with the age of the dolphins, with the liver accumulating the highest concentrations. No sex differences were observed in the mercury and selenium concentrations. While differences in tissue mercury concentrations were not observed due to the UME, the selenium accumulation profiles were significantly different between the two time periods. These results suggest that selenium may not have been as protective against mercury toxicity in the bottlenose dolphins that were stranded during the UME, possibly due to infection with morbillivirus.
... Mercury levels also vary with the diet of the dolphin, since prey can include animals at multiple trophic levels (e.g., squid, carnivorous fish) (Stavros et al., 2008;Hong et al., 2013;Baptista et al., 2016). Several previous studies have found no difference in total Hg concentrations between males and female bottlenose dolphins (Durden et al., 2007;Meador et al., 1999), while Hong et al. (2012) found that concentrations were higher in females, especially those who are pregnant or nursing. These females require increased feeding and presumably had a larger mercury intake. ...
... Study results were compared visually by graphing regressions of length versus tissue concentrations (Fig. 1) and by one-way ANCOVAs with length as a covariate. Liver concentrations did not differ significantly between this study and those also done on the Atlantic Coast in South Carolina (Beck et al., 1997) and Florida (Durden et al., 2007) or from the Canary Islands (García-Alvarez et al., 2015). Hg concentrations in muscle tissue however were significantly lower for our study relative to the dolphins studied on the Indian River Lagoon on the Atlantic Coast of Florida (Durden et al., 2007) (p = 0.003). ...
... Liver concentrations did not differ significantly between this study and those also done on the Atlantic Coast in South Carolina (Beck et al., 1997) and Florida (Durden et al., 2007) or from the Canary Islands (García-Alvarez et al., 2015). Hg concentrations in muscle tissue however were significantly lower for our study relative to the dolphins studied on the Indian River Lagoon on the Atlantic Coast of Florida (Durden et al., 2007) (p = 0.003). Hg concentrations in skin were also significantly lower for our study than for live dolphins sampled in Table 1 Mercury concentrations (mean ± SD and range; μg/g dw) in tissue of bottlenose dolphins stranded in Virginia. ...
For marine cetaceans, Hg biomagnification can negatively affect neurological, hepatic, renal, and immune functions. To evaluate the use of biomarkers for Hg in dolphins, multiple tissues were analyzed from 127 stranded common bottlenose dolphins (Tursiops truncatus) from the estuarine and oceanic waters of Virginia, USA. Twenty-two percent of liver Hg concentrations exceeded the published observed effect level for liver abnormalities, and 26 % of cerebrum samples exceeded the published threshold for neurochemical changes, suggesting that Hg may have impacted dolphin health. Mercury tissue levels were similar to or lower than those reported from other locations (liver range: 1.4–943 μg/g-dw). Significant correlations were found between tissue types, indicating that skin or liver can be used as a biomarker to estimate the total Hg concentrations in the other tissue types (kidney, liver, cerebrum, cerebellum, pons). This is the first study to measure Hg concentrations in multiple brain regions of T. truncatus.
... Previous studies have explored tissue concentrations and distributions of heavy metals and other trace elements in dolphins and toothed whales. While many studies have focused specifically on examining concentrations and molar ratios of mercury and selenium in odontocetes [30][31][32][33][34][35][36][37]; others have focused on heavy metals including mercury, cadmium, lead, and zinc [26][27][28][29][38][39][40][41][42][43]; and still others report results of extended analyses of many trace elements including essential and non-essential elements [3,4,17,[44][45][46][47][48]. Data remain sparse, however, on how specific elements become distributed within a given animal's body, especially for many rarely encountered species, and how toxicant levels relate to animal signalment and other demographic factors. ...
... have concluded that young cetaceans are unable to efficiently demethylate methylmercury, and that initiation of the demethylation process requires the total mercury concentration to reach a certain threshold value [13,34,36,94]. Another possible scenario is that maternal transfer of heavy metal contaminants results in juveniles starting life with relatively higher metals burdens, that they are then required to detoxify [33]. More recently, evidence from a study on short-finned pilot whales (Globicephala macrorhynchus) suggests that the selenium-mediated detoxification process is fully developed from an early age, and that the previously observed lack of demethylation products in tissues with total mercury concentrations below threshold values may be explained by the kinetic rates of the detoxification reactions, which are assumed to be slow based on slow distribution kinetics of dietary methylmercury between individual organs [37,95]. ...
Odontocetes obtain nutrients including essential elements through their diet and are exposed to heavy metal contaminants via ingestion of contaminated prey. We evaluated the prevalence, concentration, and tissue distribution of essential and non-essential trace elements, including heavy metal toxicants, in tissue (blubber, kidney, liver, skeletal muscle, skin) and fecal samples collected from 90 odontocetes, representing nine species, that stranded in Georgia and Florida, USA during 2007–2021. Samples were analyzed for concentrations of seven essential (cobalt, copper, iron, manganese, molybdenum, selenium, zinc) and five non-essential (arsenic, cadmium, lead, mercury, thallium) elemental analytes using inductively-coupled plasma mass spectrometry. Risso's dolphins (Grampus griseus) and short-finned pilot whales (Globicephala macrorhynchus) had the highest median concentrations of mercury, cadmium, and lead, while dwarf sperm whales (Kogia sima) had the lowest. Adult pygmy and dwarf sperm whales that stranded in 2019–2021 had higher concentrations of arsenic, copper, iron, lead, manganese, selenium, thallium, and zinc compared to those that stranded in 2010–2018, suggesting an increasing risk of exposure over time. The highest concentrations of many elements (e.g., cadmium, cobalt, copper, manganese, molybdenum, thallium, zinc) were in fecal samples, illustrating the usefulness of this noninvasively collected sample. Aside from fecal samples, hepatic tissues had the highest concentrations of iron, manganese, mercury, molybdenum, and selenium in most species; renal tissues had the highest concentrations of cadmium; skin had the highest concentrations of zinc; and copper, arsenic, and lead concentrations were primarily distributed among the liver and kidneys. Phylogenetic differences in patterns of trace element concentrations likely reflect species-specific differences in diet, trophic level, and feeding strategies, while heterogeneous distributions of elemental analytes among different organ types reflect differences in elemental biotransformation, elimination, and storage. This study illustrates the importance of monitoring toxic contaminants in stranded odontocetes, which serve as important sentinels of environmental contamination, and whose health may be linked to human health.
... Hepatic fibrosis of unknown etiology, as well as hepatic lipidosis, are common in free-ranging bottlenose dolphins and were previously observed at similar prevalences (~30% and ≥12%, respectively) [61,62,64]. Mercury bioaccumulation in bottlenose dolphins has been associated with hepatic necrosis, hepatitis, and hepatic lipidosis in western Florida [65], as well as liver enzyme elevations in the IRL [66,67], and they may have contributed to the liver lesions observed herein. Though liver neoplasia is uncommon in bottlenose dolphins, adenoma, reticuloendotheliosis, and immunoblastic malignant lymphoma have been reported [63,[68][69][70], the latter of which was associated with elevated concentrations of polychlorinated biphenyl congeners [63]. ...
Microcystin (MC), a hepatotoxin produced by cyanobacteria, was introduced into the Indian River Lagoon (IRL), Florida, in 2005 through freshwater outflows. Since then, MC has been detected in humans, domestic animals, and wildlife in the lagoon. Potential public health effects associated with MC exposure along the IRL include an increased risk of non-alcoholic liver disease among area residents. Yet, there are limited studies characterizing liver disease, as well as the potential role of MC, in humans and animals in this region. Thus, histopathology reports (n = 133) were reviewed in the stranded common bottlenose dolphin (Tursiops truncatus truncatus) (n = 156, 2005–2024) to describe liver lesions in this important IRL sentinel. Liver and fecal samples (n = 161) from stranded individuals were screened for MC via an enzyme immunoassay (ELISA). These samples were then confirmed via the 2-methyl-3-methoxy-4-phenylbutyric acid technique (MMPB) to evaluate whether liver histopathologic lesions were linked to MC exposure. Minimally invasive MC screening methods were also assessed using respiratory swabs and vapor. Inflammation (24%, n = 32), fibrosis (23%, n = 31), lipidosis/vacuolation (11%, n = 15), and necrosis (11%, n = 14) were the most common liver anomalies observed. These non-specific lesions have been reported to be associated with MC exposure in numerous species in the peer-reviewed literature. Ten bottlenose dolphins tested positive for the toxin via ELISA, including two individuals with hepatic lipidosis, but none were confirmed by MMPB. Thus, this study did not provide evidence for MC-induced liver disease in IRL bottlenose dolphins. Other causes should be considered for the lesions observed (e.g., heavy metals, metabolic disease, and endoparasites). Respiratory swabs require further validation as a pre-mortem MC screening tool in free-ranging wildlife.
... The average liver Hg level in IRL river otters was lower than the proposed background level (4 µg/g dw) for the species [45,49]. However, since high-level Hg bioaccumulation and associated liver anomalies have been observed in IRL bottlenose dolphins at levels known to be toxic to river otters and other mammals, and Hg has been suspected of impacting the stability of other river otter populations worldwide [17][18][19]21,45,50], continued Hg monitoring is recommended in the IRL population whenever feasible. ...
The harmful algal bloom (HAB) liver toxin microcystin (MC) and trace element biomagnification were previously detected in organisms in the Indian River Lagoon (IRL), Florida. Since there are no routine screening programs for these contaminants, liver tissue from North American river otters (Lontra canadensis), an important sentinel species in the IRL, was screened for MC via enzyme-linked immunoassay (ELISA), followed by confirmatory analyses via liquid-chromatography/mass spectrometry methods (LC-MS/MS). Liver and kidney samples were evaluated for trace element (As, Cd, Co, Cu, Fe, Hg, Mn, Mo, Pb, Se, Tl, and Zn) bioaccumulation via inductively coupled plasma mass spectrometry (ICP-MS). Histopathologic evaluation of the liver and kidney was conducted to assess possible correlation with toxic insults. Forty-three river otters were evaluated (2016–2022). Microcystin was not detected in any river otter sample (n = 37). Of those tested for trace element bioaccumulation (n = 22), no sample measured above provided reference ranges or estimated toxic thresholds for this species. There were no statistically significant patterns observed based on season, year, or age class, but sex had a small influence on trace element levels in the kidney. One individual had a kidney Cu level (52 μg/g dry weight) higher than any previously reported for this species. Trace elements were detected at presumed background levels providing baselines for future monitoring. For otters with available histopathologic evaluation (n = 28), anomalies indicative of contaminant exposure (non-specific inflammation, necrosis, and/or lipidosis) were present in the liver and kidney of 18% and 4% of individuals, respectively. However, since these lesions were not linked to abnormal trace element bioaccumulation or MC exposure, other causes (e.g., infectious disease) should be considered.
... In a previous study from the Adriatic Sea, stranded bottlenose dolphins had very high Hg concentrations: a 16-year old bottlenose dolphin found in the Split area had a Hg concentration of 1834 mg/kg in the liver (Pompe-Gotal et al., 2009) and a 14-year old male bottlenose dolphin found near the Island of Hvar had a liver concentration of 1790 mg/kg (Bilandžić et al., 2012). On the other hand, these levels were higher than tissues levels of bottlenose dolphins from different locations in the Atlantic Ocean, such as in USA (Meador et al., 1999;Durden et al., 2007;Stavros et al., 2011), Portugal (Carvalho et al., 2002), or the Hawaiian Islands (Hansen et al., 2016). ...
Top marine predators present high mercury concentrations in their tissues due to biomagnification in the marine food chain. This study reports mercury (Hg) and selenium (Se) status, and the Hg:Se molar ratio assessment in bottlenose (Tursiops truncatus), striped (Stenella coeruleoalba) and Risso's dolphins (Grampus griseus). Total Hg and Se concentrations were determined in muscle, liver, kidney, lung, spleen, adipose tissue and skin collected from 186 specimens stranded in the Croatian part of Adriatic Sea from 1995 to 2014. Total Hg concentrations in tissue samples ranged from 0.001 in the spleen to 2238 mg/kg wet weight in liver. Se concentrations in dolphin samples ranged from 0.010 to 2916 mg/kg ww. Minimum Se concentration was found in muscle and maximum Se concentration were found in liver of bottlenose dolphin. Hg and Se levels in Risso's dolphins showed higher concentrations in all tissues in comparison to bottlenose and striped dolphins. Significant and positive correlations were observed between age and Hg concentrations (P < 0.05). In 66.6 % of Risso's, 15.3 % of bottlenose dolphins and one stranded striped dolphin in this study, the hepatic concentration of Hg exceeded the higher toxic thresholds (400 mg/kg w.w.) previously defined as evidence of liver damage in marine mammals. The Hg:Se molar ratio in the liver of Risso's dolphin was 0.670. The liver of adult bottlenose dolphins showed expected values (0.870), while the liver of young dolphins had a high ratio (0.750), non-specific for the age group. The Hg:Se molar ratio in the liver of striped dolphins was 0.390, which is lower than the literature values.
... We examined immune function in two populations of noncaptive turtles, comparing resident turtles from an area of poor water quality with those in a more pristine environment. Florida's Indian River Lagoon (IRL) is a heavily polluted estuary with high levels of heavy metals and persistent organic pollutants (Wang et al. 1992;Durden et al. 2007;Fair et al. 2010) and eutrophication (Lapointe et al. 2015;Barile 2018). As with other animals in the IRL, resident juvenile green turtles exhibit high rates of disease, with approximately 50% of green turtles showing tumors (Hirama and Ehrhart, 2007;Lawrance et al. 2018). ...
There is a strong correlation between degraded marine habitats and the prevalence of diseases such as green turtle fibropapillomatosis (GTFP) in coastal populations. In GTFP, small to large tumors grow on the turtle's soft tissues and shell, while internal nodules may also occur. The disease primarily affects juvenile green sea turtles (Chelonia mydas) that reside in nearshore waters. As a link has been shown between environmental pollution and immune suppression in a variety of animals, the objective of our research was to compare innate and adaptive immune responsiveness in green sea turtles from a severely degraded and a more pristine habitat, which differ greatly in rates of GTFP. We quantified phagocytosis by flow cytometry and performed in vitro stimulation analysis to measure activity of both the innate and adaptive immune systems in wild-caught Florida green turtles. Sea turtles from the degraded environment, both with and without visible cutaneous tumors, exhibited significantly reduced phagocytosis and stimulation indices than did those from the less polluted environment. Our results suggest that environmental factors may contribute to the development of GTFP and thus can impact the health of sea turtle populations.
... Seagrass meadows have been found to provide critical habitat to prey consumed by estuarine dolphins [39]; therefore, these significant ecological changes are likely to jeopardize the health of the already vulnerable IRL dolphin stock. Recent studies have documented diminished health in IRL dolphins including high concentrations of mercury [40], lingual and genital papillomas [41], and skin disease (lacaziosis) [42,43]. Moreover, interactions with both commercial and recreational fisheries account for up to 12% of the annual mortality [8,44]. ...
Common bottlenose dolphins (Tursiops truncatus truncatus) inhabiting the Indian River Lagoon (IRL) estuarine system along the east coast of Florida are impacted by anthropogenic activities and have had multiple unexplained mortality events. Given this, managers need precise estimates of demographic and abundance parameters. Mark-recapture photo-identification boat-based surveys following a Robust Design were used to estimate abundance, adult survival, and temporary emigration for the IRL estuarine system stock of bottlenose dolphins. Models allowed for temporary emigration and included a parameter (time since first capture) to assess evidence for transient individuals. Surveys (n = 135) were conducted along predetermined contour and transect lines throughout the entire IRL (2016–2017). The best fitting model allowed survival to differ for residents and transients and to vary by primary period, detection to vary by secondary session, and did not include temporary emigration. Dolphin abundance was estimated from 981 (95% CI: 882–1,090) in winter to 1,078 (95% CI: 968–1,201) in summer with a mean of 1,032 (95% CI: 969–1,098). Model averaged seasonal survival rate for marked residents was 0.85–1.00. Capture probability was 0.20 to 0.42 during secondary sessions and the transient rate was estimated as 0.06 to 0.07. This study is the first Robust Design mark-recapture survey to estimate abundance for IRL dolphins and provides population estimates to improve future survey design, as well as an example of data simulation to validate and optimize sampling design. Transients likely included individuals with home ranges extending north of the IRL requiring further assessment of stock delineation. Results were similar to prior abundance estimates from line-transect aerial surveys suggesting population stability over the last decade. These results will enable managers to evaluate the impact of fisheries-related takes and provide baseline demographic parameters for the IRL dolphin population which contends with anthropogenic impacts and repeated mortality events.
Trace elements (TEs) constitute the oldest emerging pollutants globally, most occur from natural sources, but a few are derived from anthropogenic sources. Marine mammals are considered bioindicators of ecosystem contamination. The aims of this review is compile reports on essential and nonessential TEs occurrence in small cetaceans from Argentinean waters; and to review the existing information on the concentration of TEs in the Franciscana dolphin, a biomonitor species of the Argentine coastal marine ecosystem. We searched reports where levels of TEs were present in small cetaceans from and eight species were analysed: Pontoporia blainvillei, Tursiops truncatus gephyreus, Kogia breviceps, Delphinus delphis, Lagenorhynchus obscurus, Lagenodelphis hasei, Cephaloryhchus commersonii and Ziphius cavirostris. Essential TEs like Zn, Cu, Mn, Cr, Fe, Co, Ni, Mo, Se, As, Au, Ag, Sn, and nonessential TE as Pb, Cd, Hg, As was considered. The reports compiled in this article analysed kidney, liver, muscle and occasionally brain, skin, lung and spleen, covering a temporal range of 30 years, from 1982 to 2016. Of data analysis, we identify knowledge gaps, species of small cetaceans for which the concentration of trace metals is not yet known and areas on the Argentine coast where there are no reports that analyse them. The most recent information corresponds to the 2010 decade, and in those subsequent publications, the samples were taken at that time. This emphasizes the importance of reviewing this data, in order to compare old and new datasets, create contamination timelines and evaluate possible increases or decreases of contaminants in different study areas. The information recopilated will serve as valuable baselines to detect the future impact of increasing human, even natural, activities on marine ecosystems in the South Atlantic Ocean.
Mortality patterns in cetaceans are critical to understanding population health. Common bottlenose dolphins (Tursiops truncatus truncatus) inhabiting the Indian River Lagoon (IRL), Florida have been subjected to four unusual mortality events (UMEs), highlighting the need to evaluate morbidity and mortality patterns. Complete gross examinations were conducted on 392 stranded dolphins and histopathological analyses were conducted for 178 animals (2002-2020). The probable causes of mortality were grouped by etiologic category: degenerative, metabolic, nutritional, inflammatory (infectious and noninfectious disease), and trauma. Probable cause of mortality was determined in 57% (223/392) of cases. Inflammatory disease (infectious/noninfectious) and trauma were the most common. Inflammatory disease accounted for 41% of cases (91/223), with the lungs (pneumonia) most commonly affected. Trauma accounted for 36% of strandings (80/223). The majority of trauma cases were due to anthropogenic activities (entanglement, fishing gear or other debris ingestion, and propeller strikes), accounting for 58% of trauma cases (46/80). Natural trauma (prey-associated esophageal obstruction or asphyxiation, shark bites, and stingray interactions) accounted for 12% of all cases (26/223), and trauma of undetermined origin was identified in 4% of cases (8/223). Starvation or inanition (nutritional) were the probable cause of mortality in 17% of cases and peaked during the 2013 UME (61% of cases). Degenerative and metabolic etiologies accounted for 5% of cases. This study represents the most comprehensive evaluation of morbidity and mortality patterns in IRL dolphins. Because IRL dolphins are routinely exposed to anthropogenic threats and have endured multiple UMEs, these baseline data are critical to the conservation and management of this population.
Research was carried out on a 21-year-old, 288 cm-long free-living grand multigravida female bottlenose dolphin (Tursiops truncatus, Montagu 1821) with mass of 214 kg. The animal died on 8 October 1997 in the Adriatic Sea, near Šibenik, Croatia. Prior to death she showed some neurological symptoms. For control and comparison we used the carcasses and tissues of two presumably clinically healthy dolphins. Autopsy showed massive edema in the subcutaneous tissues (between blubber and musculature) on the dorsal side of the body of the diseased subject. The fluid in intercellular tissue spaces was clear and light-yellowish. Larger amounts of the same fluid were found in serous sacs of the animal, as well as slight brain edema. The most prominent structural change was found in the liver, which was normal in size but extremely yellow and fragile. Its structure was totally destroyed, without any traces of blood, and there was pronounced fatty degeneration of liver parenchyma. All hepatocytes were also destroyed and swollen mitochondria and dilated endoplasmic reticulum were evident. This massive hepatic degeneration and necrosis was probably due to some unknown acute biological or chemical agent that provoked hepatargic crisis and the ultimate death of this free-living female dolphin.
