Article

Bioaccumulation of toxic metals in loggerhead turtles from Mediterranean Sea coast, Egypt

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Abstract

Heavy metal concentrations in the different tissues of marine turtles are presented; the most frequently monitored elements are mercury, cadmium and lead. Concentrations of Hg, Cd, Pb and As in different organs and tissues (liver, kidney, muscle tissue, fat tissue and blood) of loggerhead turtles Caretta caretta from south eastern Mediterranean Sea were determined. The highest levels of cadmium and arsenic were found in kidney (Cd: 61.17 μg g-1; As: 0.051 μg g-1dry weight). For lead the highest level was found in muscle tissue (35.80 μg g-1). Mercury tended to be higher in liver than in other tissues and organs (0.253 μg g-1 dry weight) which showed a higher accumulation of this element. Fat tissue generally displayed the lowest trace element burdens. The concentrations of As remained low in all the considered tissues, possibly the result of low trophic level in sea turtles. In contrast, the diet of loggerhead turtles would result in a significant exposure to Pb. This is the first study into metal accumulation in tissues of loggerhead turtle from Egyptian Mediterranean coastline.

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... The principal explanation for this tendency is the prohibition of leaded gasoline, increase of wastewater treatment and diversity of dischargers to oceans (Orisakwem et al., 2014;Solaun et al., 2013;Von et al., 2003); these actions were implemented in the 1990's and the early 2000's in many countries. A final important point was that (Abdallah and Abd-Allah, 2011) had the highest reports of these 3 non-essential metals in Loggerhead turtles from the Egyptian Mediterranean, which should be an alarm signal regarding the pollution of this area. Other elements commonly analyzed were Zn, Cu, Se, As and Ni; Cr, Al and Mn were studied less frequently. ...
... Cadmium and Pb also had low concentrations in this tissue; Frias-Espericueta et al. (2006) reported one of the highest Cd and Pb concentrations (2.6 and 1.78 mg g À1 ww respectively) in L. olivacea from Mexico. Torrent et al. (2004) and Abdallah and Abd-Allah (2011) had the highest reports for Pb with 2.26 (Canary Islands) and 2.24 (Mediterranean) mg g À1 ww respectively, both in C. caretta. In Fig. S5a the NEA area (Canary Islands included) has a slight upward trend compared with other RMUs. ...
Article
Inorganic elements (Pb, Cd, Hg, Al, As, Cr, Cu, Fe, Mn, Ni, Se and Zn) are present globally in aquatic systems and their potential transfer to marine turtles can be a serious threat to their health status. The environmental fate of these contaminants may be traced by the analysis of turtle tissues. Loggerhead turtles (Caretta caretta) are the most frequently investigated of all the sea turtle species with regards to inorganic elements, followed by Green turtles (Chelonia mydas); all the other species have considerably fewer studies. Literature shows that blood, liver, kidney and muscle are the tissues most frequently used for the quantification of inorganic elements, with Pb, Cd, Cu and Zn being the most studied elements. Chelonia mydas showed the highest concentrations of Cr in muscle (4.8 ± 0.12), Cu in liver (37 ± 7) and Mg in kidney (17 mg g 1 ww), Cr and Cu from the Gulf of Mexico and Mg from Japanese coasts; Lep- idochelys olivacea presented the highest concentrations of Pb in blood (4.46 5) and Cd in kidney (150 ± 110 mg g 1 ww), both from the Mexican Pacific; Caretta caretta from the Mediterranean Egyptian coast had the highest report of Hg in blood (0.66 ± 0.13 mg g 1 ww); and Eretmochelys imbricata from Japan had the highest concentration of As in muscle (30 ± 13 13 mg g 1 ww). The meta-analysis allows us to examine some features that were not visible when data was analyzed alone. For instance, Leatherbacks show a unique pattern of concentration compared to other species. Additionally, contamination of different tissues shows some tendencies independent of the species with liver and kidney on one side and bone on the other being different from other tissues. This review provides a general perspective on the accumulation and distribution of these inorganic elements alongside existing information for the 7 sea turtle species.
... Green turtle reference intervals established in Northeastern Brazil have also found lower concentrations of trace elements (Agostinho et al., 2020). However, loggerhead sea turtles have a more carnivorous diet than green turtles (Tomas et al., 2001), and previous reviews and research on trace element concentrations in turtles have found the highest concentrations of lead, cadmium and mercury in loggerhead sea turtles (Abdallah and Abd-Allah, 2011;Cortes-Gomez et al., 2017;Ley-Quiñónez et al., 2011). ...
... Very low As concentrations were detected in this study, in contrast to what was found in Loggerhead sea turtles stranded in the South Adriatic Sea (15.47 ± 11.91 mg/kg w.w.) (Storelli et al. 1998;Storelli and Marcotrigiano 2000), Portugal (14.7 ± 1.47 mg/kg w.w.) (Nicolau et al. 2017) and Canarias (7.35 ± 1.37 mg/kg w.w.) (Torrent et al. 2004), even though the diet of southeast Mediterranean Loggerhead sea turtles is primarily based on small crustaceans which usually show high concentrations of total As (Norin et al. 1985;Godley et al. 1997). Our findings on As concentrations seem to be similar to what was found by Abdallah and Abd-Allah (2010) in Loggerhead sea turtles stranded on Egyptian coasts. Besides dietary differences, bioaccumulation of contaminants in marine biota can be viewed as a result of the interaction of numerous biological factors comprising age, trophic level, locality of sampling, and reproductive state (Storelli and Zizzo 2014;Cammilleri et al. 2017). ...
Article
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Background The Loggerhead sea turtle (Caretta caretta) is a marine reptile belonging to a monophyletic group of chelonians. As these animals are long-lived, they have the ability to accumulate pollutants. Aim To collect epidemiological data on toxic metals in marine Loggerhead sea turtles. Materials and Methods Forty Loggerhead sea turtles comprising 25 males and 15 females stranded freshly dead between 2013 and 2018 along the coasts of Sicily, Southern Italy, were examined for arsenic, cadmium, and lead accumulation in muscle and adipose tissues by means of a validated ICP-MS method. A modified K index as a growth condition factor, namely Fulton’s K index, was used. Samples were tested in duplicate. A Wilcoxon rank sum test was carried out to evaluate metal contents differences between muscle and adipose tissues and between genders. Results The Fulton’s K index suggested a good body condition of the C. caretta recovered with mean values of 5.34 ± 3.40 (n = 40; ±SD). Detectable concentrations of lead were found in 70% of the samples analysed with mean values of 0.65 ± 1.67 mg/kg wet weight and 0.51 ± 1.29 mg/kg wet weight in muscle and adipose tissues, respectively. No significant differences in arsenic, cadmium, and lead were detected between genders. In addition, no significant correlation was found between modified K index and concentrations of arsenic, cadmium, and lead. Clinical relevance Findings on muscle and adipose tissues suggest chronic exposure of Caretta caretta to high concentrations of especially lead which might negatively affect health and welfare of these marine turtles although body condition was good.
... While our results were nearly within the limits of previously published studies (Table 3), some elements were found in higher concentrations. For instance, when compared to previous studies (Torrent et al., 2004;Abdallah and Abd-Allah, 2011;Yipel et al., 2017), we observed the highest Al concentrations measured for all tissues in subadult individuals of both studied species along the Northern Cyprus coast and the highest As concentrations in green turtle livers described in the literature (Saeki et al., 2000;Kaska et al., 2004;Lam et al., 2004;Faust et al., 2014). ...
Article
Sea turtles are considered pollution bioindicators due to their tendency to accumulate high metal levels in their tissues during their long lifespans. In this context, we aimed to analyse the concentrations of 12 elements in liver, kidney, heart and muscle samples from green turtles (Chelonia mydas; n = 41) and loggerhead turtles (Caretta caretta; n = 14) found stranded in Northern Cyprus. The samples were collected between 2019 and 2021, stored in sterile Eppendorf tubes at −20 °C until metal analysis, and analysed with an inductively coupled plasma mass spectrometer. With this study, we contribute to the limited number of studies on metal accumulation in heart tissue and present the first data for Mg accumulation in the heart, liver, muscle and kidney tissues of both species. We found that metal accumulation levels differed among the two study species’ tissues, with some elements in the same tissue (AlKidney, AsHeart, AsLiver, FeMuscle, FeKidney, FeHeart, MnHeart, PbHeart, ZnMuscle and ZnKidney) significantly differing between species. The observed variation likely resulted from their different feeding habits, which cause them to be exposed to different levels of metals. We also found significant associations among elements within tissues, as well as between the same element across different tissues in both species, which may indicate the differential accumulation of elements among organs due to physiological processes in turtle metabolism, bioaccumulation or excretion.
... While our results were nearly within the limits of previously published studies (Table 3), some elements were found in higher concentrations. For instance, when compared to previous studies (Torrent et al., 2004;Abdallah and Abd-Allah, 2011;Yipel et al., 2017), we observed the highest Al concentrations measured for all tissues in subadult individuals of both studied species along the Northern Cyprus coast and the highest As concentrations in green turtle livers described in the literature (Saeki et al., 2000;Kaska et al., 2004;Lam et al., 2004;Faust et al., 2014). ...
Thesis
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Long-lived marine species such as marine turtles are becoming an important tool in ecotoxicology because of their sensitivity to marine environmental change, especially regarding pollution. They usually occupy diverse trophic levels in the marine food web (depending on the age and species), and can therefore accumulate different pollutants over their lifetimes in different ecological niches (Aguirre and Lutz, 2004; Camacho et al., 2013b). Turtle blood is thought to be a good tool for the simultaneous monitoring of environmental contaminants and clinical parameters (Camacho et al., 2013b). However, only the elements of a recent exposition can be found in blood (acute exposure). In order to better elucidate the chronic exposure and accumulation of these elements, it is still necessary to use their accumulation target organs. Inorganic elements, on the other hand, such as Pb, Cd, Cu As, Se and Ni, have been proven to provoke toxicological effects in many aquatic animal species, but marine turtles have been little investigated in this regard. Thus, the aim of this Doctoral Thesis was to evaluate the concentration of inorganic elements in blood and tissues (liver kidney, bone, muscle, brain and fat) from a large number of Lepidochelys olivacea turtles (241 nesting marine turtles and tissues from 58 dead turtles) from La Escobilla beach (Oaxaca, Mexico). In this manner, the actual situation of this population in this area could be analyzed, alongside different possible molecular, biochemical and anatomical biomarkers to assess their possible utility regarding turtle health and their relation with these inorganic elements over 3 years (2012-2014). The first part of the Introduction (section 1.1) describes the principal characteristics of the Olive Ridley turtles and La Escobilla beach. This section touches upon the ecological importance of marine turtles, the morphological characteristics of the studied species, their feeding habits, reproductive behaviour, distribution, habitats and their principal threats. The second part of the introduction (Chapter I) is a state of the art review and meta-analysis of the most studied inorganic elements worldwide (Pb, Cd, Hg, Al, As, Cr, Cu, Fe, Mn, Ni, Se and Zn) for the 7 marine turtle species. We show that all these elements are above the detection limit, at least in some individuals of all the species and populations studied. This meta-analysis also showed some features of contamination, and the distribution of these pollutants regarding sea basins, species and tissues. In the Experimental Chapters, the first part (Biomonitoring) contains 2 sections (Chapters II and III). Here, the concentrations of 14 inorganic elements in the blood of 241 live turtles and different tissues (liver, kidney, muscle, brain, bone, fat and blood) of 58 dead turtles are described. These samples were taken over three different years during 8 different arribadas. The results of this biomonitoring program allow us to better understand the distribution of these elements; this was especially informative for some elements not commonly analyzed (Sr, Ti, Tl). An alarming level of Cd was also found in this population. A decreasing tendency in many of these inorganic elements through those three years was also observed. Since blood is commonly used in biomonitoring programs, the relationship between blood and tissues of dead individuals was also tested to check if there were significant relationships that might indicate that blood could be used to predict the accumulation of these elements in tissues. The second part of the Experimental Chapters (Biomarkers) runs from chapters IV to VII. These sections (3.1 to 3.5) contain studies evaluating commonly used biomarkers in many species to determine the effects of inorganic elements on the health of the animals, although they have been little studied in marine turtles and none of them have been previously described in Lepidochelys olivacea. Additionally, a possible new biomarker using the asymmetry of the carapace of these turtles was developed. Firstly, molecular biomarkers were studied (section 3.3): the presence of metallothionein (MT), superoxide dismutase (SOD), catalase (CAT) and glutathione reductase (GR) transcription and/or enzymatic activities related to some inorganic elements (Al, As, Cd, Cr, Cu, Fe, Li, Ni, Pb, Sb, Se, Sr, Ti, Tl and Zn) was determined. The most common biochemical analytes related to pollutants were also determined (sections 3.4.1 and 3.4.2) through biochemical analysis in serum samples from two different years. ALT, AST, ALP, albumin, creatinine, glucose, urea, cholesterol, cortisol and esterase activity (EA) were determined in samples from two years (2013 and 2014). These biochemical parameters were also related to some inorganic elements (As, Cd, Cr, Mn, Ni, Pb, Sr, Ti, Zn and Se). In the final chapter of this Thesis (VIII), a new tool for measuring the asymmetry of the carapace was developed (DIx) and related to the concentrations of 15 inorganic elements (Bi, Cd, Li, Pb, Sb, Sr, Ti, Tl, Al, As, Co, Cr, Cu, Ni, and Se) from 17 dead turtles (blood, liver, kidney, muscle, fat, bone, brain and egg parts). Lepidochelys olivacea is characterized by remarkable morphological variability in the number and shape of scutes, the origin of which is thought to be based on a permissive genetic background. The influence of pollutants on developmental instability and one of its consequences, the asymmetry of individuals, has been demonstrated in several species. However, the use of this asymmetry as a biomarker of contamination in adult individuals has never been explored. Thus, we developed an index to quantify developmental instability (DIx) based on the number and relative size of costal carapace scutes. The link between DIx inorganic element concentrations was then explored in various tissues and egg components of stranded dead Olive Ridley females from the Southern Pacific coast of Mexico (3 arribadas from 2014).
Chapter
Anthropogenic input of chemical pollutants into the marine environment has led to substantial increases in the concentrations of naturally occurring trace metals. Related to this there is a growing concern regarding the occurrence of these elements in marine organisms and their hazard potential. In Latin America six of seven sea turtle species inhabit the coastal areas, and many studies evaluated the concentrations of metals in blood, tissues, eggs, and hatchlings of these animals. However, information for many countries is still unknown. Considering the results from all studies, a clear organotropism is found with higher levels of Cu, Mn, Pb, and Hg in the liver and Cd and As in the kidney. In blood, the highest concentration of Cd was from Mexican Lepidochelys olivacea. Chelonia mydas from Brazil showed the highest Pb and As levels, while Eretmochelys imbricata had the highest concentration of Hg. In eggs, the highest load of metals was incorporated in the yolk. Some publications correlated the contaminant levels with biochemical parameters, oxidative stress, and diseases. This chapter is a review of the available toxicological research and the biomarkers used as indicators of metal exposure in sea turtles from Latin America.
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