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Trace element reference intervals in the blood of healthy green sea turtles to evaluate exposure of coastal populations
2017
Villa, C.A. | Flint, M. | Bell, I. | Hof, C. | Limpus, C.J. | Gaus, C.
Exposure to essential and non-essential elements may be elevated for green sea turtles (Chelonia mydas) that forage close to shore. Biomonitoring of trace elements in turtle blood can identify temporal trends over repeated sampling events, but any interpretation of potential health risks due to an elevated exposure first requires a comparison against a baseline. This study aims to use clinical reference interval (RI) methods to produce exposure baseline limits for essential and non-essential elements (Na, Mg, K, Ca, Ti, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Mo, Cd, Sb, Ba, and Pb) using blood from healthy subadult turtles foraging in a remote and offshore part of the Great Barrier Reef. Subsequent blood biomonitoring of three additional coastal populations, which forage in areas dominated by agricultural, urban and military activities, showed clear habitat-specific differences in blood metal profiles relative to the those observed in the offshore population. Coastal turtles were most often found to have elevated concentrations of Co, Mo, Mn, Mg, Na, As, Sb, and Pb relative to the corresponding RIs. In particular, blood from turtles from the agricultural site had Co concentrations ranging from 160 to 840 μg/L (4–25 times above RI), which are within the order expected to elicit acute effects in many vertebrates. Additional clinical blood biochemistry and haematology results indicate signs of a systemic disease and the prevalence of an active inflammatory response in a high proportion (44%) of turtles from the agricultural site. Elevated Co, Sb, and Mn in the blood of these turtles significantly correlated with elevated markers of acute inflammation (total white cell counts) and liver dysfunction (alkaline phosphatase and total bilirubin). The results of this study support the notion that elevated trace element exposures may be adversely affecting the health of nearshore green sea turtles.
Show more [+] Less [-]Non-destructive techniques for biomonitoring of spatial, temporal, and demographic patterns of mercury bioaccumulation and maternal transfer in turtles
2013
Hopkins, Brittney C. | Hepner, Mark J. | Hopkins, William A.
Mercury (Hg) is a globally ubiquitous pollutant that has received much attention due to its toxicity to humans and wildlife. The development of non-destructive sampling techniques is a critical step for sustainable monitoring of Hg accumulation. We evaluated the efficacy of non-destructive sampling techniques and assessed spatial, temporal, and demographic factors that influence Hg bioaccumulation in turtles. We collected muscle, blood, nail, and eggs from snapping turtles (Chelydra serpentina) inhabiting an Hg contaminated river. As predicted, all Hg tissue concentrations strongly and positively correlated with each other. Additionally, we validated our mathematical models against two additional Hg contaminated locations and found that tissue relationships developed from the validation sites did not significantly differ from those generated from the original sampling site. The models provided herein will be useful for a wide array of systems where biomonitoring of Hg in turtles needs to be accomplished in a conservation-minded fashion.
Show more [+] Less [-]Coal combustion residues and their effects on trace element accumulation and health indices of eastern mud turtles (Kinosternon subrubrum)
2018
Cochran, Jarad P. | Haskins, David L. | Eady, Naya A. | Hamilton, Matthew T. | Pilgrim, Melissa A. | Tuberville, Tracey D.
Coal combustion is a major energy source in the US. The solid waste product of coal combustion, coal combustion residue (CCR), contains potentially toxic trace elements. Before 1980, the US primarily disposed of CCR in aquatic settling basins. Animals use these basins as habitat and can be exposed to CCR, potentially affecting their physiology. To investigate the effects of CCR on eastern mud turtles (Kinosternon subrubrum), we sampled 30 turtles exposed to CCRs and 17 unexposed turtles captured in 2015–2016 from the Savannah River Site (Aiken, SC, USA). For captured turtles, we (1) quantified accumulation of CCR in claw and blood samples, (2) used bacterial killing assays to assess influences of CCR on immune responses, (3) compared hemogregarine parasite loads, and (4) compared metabolic rates via flow-through respirometry between CCR-exposed and unexposed turtles when increased temperature was introduced as an added stressor. Turtles exposed to CCR accumulated CCR-associated trace elements, corroborating previous studies. Blood Se and Sr levels and claw As, Se, and Sr levels were significantly higher in turtles from contaminated sites. Average bacterial killing efficiency was not significantly different between groups. Neither prevalence nor average parasite load significantly differed between CCR-exposed and reference turtles, although parasite load increased with turtle size. Regardless of site, temperature had a significant impact on turtle metabolic rates; as temperature increased, turtle metabolic rates increased. The effect of temperature on turtle metabolic rates was less pronounced for CCR-exposed turtles, which resulted in CCR-exposed turtles having lower metabolic rates than reference turtles at 30 and 35 °C. Our results demonstrate that turtles accumulate CCR from their environment and that accumulation of CCR is associated with changes in turtle physiological functions when additional stressors are present.
Show more [+] Less [-]Accumulation of coal combustion residues and their immunological effects in the yellow-bellied slider (Trachemys scripta scripta)
2017
Haskins, David L. | Hamilton, Matthew T. | Jones, Amanda L. | Finger, John W. | Bringolf, Robert B. | Tuberville, Tracey D.
Anthropogenic activities such as industrial processes often produce copious amounts of contaminants that have the potential to negatively impact growth, survival, and reproduction of exposed wildlife. Coal combustion residues (CCRs) represent a major source of pollutants globally, resulting in the release of potentially harmful trace elements such as arsenic (As), cadmium (Cd), and selenium (Se) into the environment. In the United States, CCRs are typically stored in aquatic settling basins that may become attractive nuisances to wildlife. Trace element contaminants, such as CCRs, may pose a threat to biota yet little is known about their sublethal effects on reptiles. To assess the effects of CCR exposure in turtles, we sampled 81 yellow-bellied sliders (Trachemys scripta scripta) in 2014–2015 from CCR-contaminated and uncontaminated reference wetlands located on the Savannah River Site (Aiken, SC, USA). Specific aims were to (1) compare the accumulation of trace elements in T. s. scripta claw and blood samples between reference and CCR-contaminated site types, (2) evaluate potential immunological effects of CCRs via bacterial killing assays and phytohaemagglutinin (PHA) assays, and (3) quantify differences in hemogregarine parasite loads between site types. Claw As, Cd, copper (Cu), and Se (all p ≤ 0.001) and blood As, Cu, Se, and strontium (Sr; p ≤ 0.015) were significantly elevated in turtles from CCR-contaminated wetlands compared to turtles from reference wetlands. Turtles from reference wetlands exhibited lower bacterial killing (p = 0.015) abilities than individuals from contaminated sites but neither PHA responses (p = 0.566) nor parasite loads (p = 0.980) differed by site type. Despite relatively high CCR body burdens, sliders did not exhibit apparent impairment of immunological response or parasite load. In addition, the high correlation between claw and blood concentrations within individuals suggests that nonlethal tissue sampling may be useful for monitoring CCR exposure in turtles.
Show more [+] Less [-]Influence of relative trophic position and carbon source on selenium bioaccumulation in turtles from a coal fly-ash spill site
2013
Van Dyke, James U. | Hopkins, William A. | Jackson, Brian P.
Selenium (Se) is a bioaccumulative constituent of coal fly-ash that can disrupt reproduction of oviparous wildlife. In food webs, the greatest enrichment of Se occurs at the lowest trophic levels, making it readily bioavailable to higher consumers. However, subsequent enrichment at higher trophic levels is less pronounced, leading to mixed tendencies for Se to biomagnify. We used stable isotopes (15N and 13C) in claws to infer relative trophic positions and relative carbon sources, respectively, of seven turtle species near the site of a recently-remediated coal fly-ash spill. We then tested whether Se concentrations differed with relative trophic position or relative carbon source. We did not observe a strong relationship between δ15N and Se concentration. Instead, selenium concentrations decreased with increasing δ13C among species. Therefore, in an assemblage of closely-related aquatic vertebrates, relative carbon source was a better predictor of Se bioaccumulation than was relative trophic position.
Show more [+] Less [-]Two decades of monitoring in marine debris ingestion in loggerhead sea turtle, Caretta caretta, from the western Mediterranean
2019
Domènech, F. | Aznar, F.J. | Raga, J.A. | Tomas, J.
Anthropogenic marine debris is one of the major worldwide threats to marine ecosystems. The EU Marine Strategy Framework Directive (MSFD) has established a protocol for data collection on marine debris from the gut contents of the loggerhead sea turtle (Caretta caretta), and for determining assessment values of plastics for Good Environmental Status (GES). GES values are calculated as percent turtles having more than average plastic weight per turtle. In the present study, we quantify marine debris ingestion in 155 loggerhead sea turtles collected in the period 1995–2016 in waters of western Mediterranean (North-east Spain). The study aims (1) to update and standardize debris ingestion data available from this area, (2) to analyse this issue over two decades using Zero-altered (hurdle) models and (3) to provide new data to compare the only GES value available (off Italian waters). The composition of marine debris (occurrence and amounts of different categories) was similar to that found in other studies for the western Mediterranean and their amounts seem not to be an important threat to turtle survival in the region. Model results suggest that, in the study area, (a) period of stranding or capture, (b) turtle size and (c) latitude are significant predictors of anthropogenic debris ingestion (occurrence and amount) in turtles. The GES value for late juvenile turtles (CCL>40 cm) has decreased in the last ten years in the study area, and this is very similar to that obtained in Italian waters. We also provide a GES value for early juvenile turtles (CCL≤40 cm) for the first time. Recommendations arising from this study include ensuring use of (1) the standardized protocol proposed by the MSFD for assessing marine debris ingestion by loggerhead sea turtles and (2) the ecology of the turtles (neritic vs oceanic), rather than their size, to obtain GES values.
Show more [+] Less [-]Integrative demographic modeling reveals population level impacts of PCB toxicity to juvenile snapping turtles
2014
Salice, Christopher J. | Rowe, Christopher L. | Eisenreich, Karen M.
A significant challenge in ecotoxicology and risk assessment lies in placing observed contaminant effects in a meaningful ecological context. Polychlorinated biphenyls (PCBs) have been shown to affect juvenile snapping turtle survival and growth but the ecological significance of these effects is difficult to discern without a formal, population-level assessment. We used a demographic matrix model to explore the potential population-level effects of PCBs on turtles. Our model showed that effects of PCBs on juvenile survival, growth and size at hatching could translate to negative effects at the population level despite the fact that these life cycle components do not typically contribute strongly to population level processes. This research points to the utility of using integrative demographic modeling approaches to better understand contaminant effects in wildlife. The results indicate that population-level effects are only evident after several years, suggesting that for long-lived species, detecting adverse contaminant effects could prove challenging.
Show more [+] Less [-]Maternal transfer and embryonic assimilation of trace elements in freshwater turtles after remediation of a coal fly-ash spill
2014
Van Dyke, James U. | Steen, David A. | Jackson, Brian P. | Hopkins, William A.
Oviparous vertebrates maternally transfer elements to their offspring during egg production. Maternal transfer occurs because elements mimic, or are incorporated into, nutrients allocated to eggs, but likely differs among species depending on the quantities of specific nutrients allocated to eggs. Developing embryos are often assumed to assimilate all of the elements allocated to eggs, but this assumption has rarely been tested. We tested the hypothesis that maternal transfer and embryonic assimilation of trace elements differed between two species of freshwater turtles exposed to a recently-remediated coal fly-ash spill. Sternotherus odoratus transferred As, Se, and Zn, while Trachemys scripta transferred As, Hg, Se, Sr, and Zn. Logarithmic non-linear relationships between hatchling and egg concentrations indicated that turtles partially assimilated elements present in eggs. In systems contaminated with multiple trace elements, our data show that maternal transfer and embryonic assimilation are element- and species-specific, and may be inconsistent even among closely-related species.
Show more [+] Less [-]Exploratory study using proton induced X-ray emission analysis and histopathological techniques to determine the toxic burden of environmental pollutants
2012
The aim of this novel research was to determine the toxic burden of increased elements in water resources on the inhabitant wild animals (squirrels, turtles, bats), using particle induced x-ray emission (PIXE) and histopathological approaches. PIXE analysis of skin, muscle, lung, liver and kidney revealed significant increase in Al, Cl, Fe, Mg, Mn, Si and V. Moreover, data clearly reflect a significant (P < 0.001) deposition of toxic elements (Al, Cl, Fe and K) in the lung producing interstitial/proliferative pneumonitis, intra-alveolar hemorrhages, and thickening of alveolar capillary walls. The results obtained from the liver samples emphasized that majority of the animals were intoxicated with Cl, Mg, S, Si and V, which have produced profound deterioration and swelling of the hepatocytes. Likewise, histopathology of the kidney sections spotlighted severe nephritis and degenerative changes, which could be associated with the elevated amount of Al, Cl and Mg. This data undoubtedly provide relevant information on the heavy burden of toxic elements and their pathological outcomes in wild animals and highlight their potential risks for human exposure. Thus, the information provided is critical for developing effective strategies in dealing with health hazards associated with elemental exposures.
Show more [+] Less [-]Quantitative overview of marine debris ingested by marine megafauna
2020
Kuhn, Susanne | van Franeker, Jan Andries
This review quantifies plastic interaction in marine biota. Firstly, entanglement and ingestion records for all marine birds, mammals, turtles, fish, and invertebrate species, are summarized from 747 studies. Marine debris affected 914 species through entanglement and/or ingestion. Ingestion was recorded for 701 species, entanglement was documented for 354 species. Secondly, the frequency of occurrence of ingestion per species (Sp-%FO) was extracted for marine birds, mammals and turtles. Thirdly, for seabird species, average numbers of plastics ingested per individual were determined. Highest Sp-%FO and average number of plastics were found in tubenosed seabirds with 41% of all birds analysed having plastics, on average 9.9 particles per bird. The Sp-%FO and average number of ingested particles is lower for most other species. However, for certain species, ingestion rates of litter are reason for serious concern. Standardized methods are crucial for future studies, to generate datasets that allow higher level ecosystem analyses.
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