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Examining the relationships between blubber steroid hormones and persistent organic pollutants in common bottlenose dolphins
2019
Galligan, Thomas M. | Balmer, Brian C. | Schwacke, Lori H. | Bolton, Jennie L. | Quigley, Brian M. | Rosel, Patricia E. | Ylitalo, Gina M. | Boggs, Ashley S.P.
Odontocete cetaceans bioaccumulate high concentrations of endocrine disrupting persistent organic pollutants (POPs), including dichlorodiphenyltrichloroethane (DDT), dichlorodiphenyltrichloroethylene (DDE), and dichlorodiphenyldichloroethane (DDD) – collectively DDTs – but few studies have explored DDTs-mediated endocrine disruption in cetaceans. Herein, we use remotely collected blubber biopsies from common bottlenose dolphins (Tursiops truncatus) inhabiting a site with high localized DDTs contamination to study the relationships between DDTs exposure and steroid hormone homeostasis in cetaceans. We quantified blubber steroid hormone concentrations by liquid chromatography-tandem mass spectrometry and blubber POP concentrations by gas chromatography-mass spectrometry. We detected six steroid hormones in blubber, including progesterone (P4), 17-hydroxyprogesterone (17OHP4), androstenedione (AE), testosterone (T), cortisol (F), and cortisone (E). Sampled dolphins (n = 62) exhibited exposure to DDT, DDE, DDD, chlordanes (CHLDs), mirex, dieldrin, hexachlorobenzene, polychlorinated biphenyls (PCBs), and brominated diphenyl ethers (BDEs). Using principal components analysis (PCA), we determined that blubber DDTs primarily loaded to the first principal component (PC1) explaining 81.6% of the total variance in POP exposure, while the remaining POPs primarily loaded to the PC2 (10.4% of variance). PC1 scores were negatively correlated with blubber T in males and blubber F in females, suggesting that exposure to DDTs impacted androgen and corticosteroid homeostasis. These conclusions were further supported by observed negative correlations between T and o,p’-DDE, o,p’-DDD, and p,p’-DDD in males sampled in the fall, and between F and the six individual DDTs and ∑6DDTs in females. Overall, these results suggest that POP-mediated endocrine disruption may have occurred in this stock of dolphins, which could negatively impact their health and fitness. However, this study relied on uncontrolled incidental exposures, making it impossible to establish a causal relationship between DDTs exposure and endocrine effects. Importantly, this study demonstrates that remotely collected blubber biopsies are a useful matrix for studying endocrine disruption in marine mammals.
Show more [+] Less [-]Bioaccumulation of organic pollutants in Indo-Pacific humpback dolphin: A review on current knowledge and future prospects
2018
Sanganyado, Edmond | Rajput, Imran Rashid | Liu, Wenhua
Indo-Pacific humpback dolphin (Sousa chinensis) are chronically exposed to organic pollutants since they inhabit shallow coastal waters that are often impacted by anthropogenic activities. The aim of this review was to evaluate existing knowledge on the occurrence of organic pollutants in Indo-Pacific humpback dolphins, identify knowledge gaps, and offer recommendations for future research directions. We discussed the trends in the bioaccumulation of organic pollutants in Indo-Pacific humpback dolphins focusing on sources, physicochemical properties, and usage patterns. Furthermore, we examined factors that influence bioaccumulation such as gender, age, dietary intake and tissue-specific distribution. Studies on bioaccumulation in Indo-Pacific humpback dolphin remain scarce, despite high concentrations above 13,000 ng/g lw we previously detected for PFOS, ∑PBDE and chlorinated paraffins. The maximum concentration of organochlorines detected was 157,000 ng/g wt. Furthermore, variations in bioaccumulation were shown to be caused by factors such as usage patterns and physicochemical properties of the pollutant. However, restrictions in sampling inhibit investigations on exposure pathway and toxicity of organic pollutants in Indo-Pacific humpback dolphin. We proposed the use of biopsy sampling, predictive bioaccumulation and toxicity modeling, and monitoring other emerging contaminants such as microplastics and pharmaceuticals for future health risk assessment on this critically endangered marine mammal species.
Show more [+] Less [-]Relationships of mercury concentrations across tissue types, muscle regions and fins for two shark species
2017
Mercury (Hg) exposure poses a threat to both fish and human health. Sharks are known to bioaccumulate Hg, however, little is known regarding how Hg is distributed between different tissue groups (e.g. muscle regions, organs). Here we evaluated total mercury (THg) concentrations from eight muscle regions, four fins (first dorsal, left and right pectorals, caudal-from both the inner core and trailing margin of each fin), and five internal organs (liver, kidney, spleen, heart, epigonal organ) from two different shark species, bonnethead (Sphyrna tiburo) and silky shark (Carcharhinus falciformis) to determine the relationships of THg concentrations between and within tissue groups. Total Hg concentrations were highest in the eight muscle regions with no significant differences in THg concentrations between the different muscle regions and muscle types (red and white). Results from tissue collected from any muscle region would be representative of all muscle sample locations. Total Hg concentrations were lowest in samples taken from the fin inner core of the first dorsal, pectoral, and caudal (lower lobe) fins. Mercury concentrations for samples taken from the trailing margin of the dorsal, pectoral, and caudal fins (upper and lower lobe) were also not significantly different from each other for both species. Significant relationships were found between THg concentrations in dorsal axial muscle tissue and the fin inner core, liver, kidney, spleen and heart for both species as well as the THg concentrations between the dorsal fin trailing margin and the heart for the silky shark and all other sampled tissue types for the bonnethead shark. Our results suggest that biopsy sampling of dorsal muscle can provide data that can effectively estimate THg concentrations in specific organs without using more invasive, or lethal methods.
Show more [+] Less [-]Linking pollutant exposure of humpback whales breeding in the Indian Ocean to their feeding habits and feeding areas off Antarctica
2017
Dāsa, Kr̥shṇā | Malarvannan, Govindan | Dirtu, Alin | Dulau, Violaine | Dumont, Magali | Lepoint, Gilles | Mongin, Philippe | Covaci, Adrian
Humpback whales, Megaptera novaeangliae, breeding off la Reunion Island (Indian Ocean) undergo large-scale seasonal migrations between summer feeding grounds near Antarctica and their reproductive winter grounds in the Indian Ocean. The main scope of the current study was to investigate chemical exposure of humpback whales breeding in the Indian Ocean by providing the first published data on this breeding stock concerning persistent organic pollutants (POPs), namely polychlorinated biphenyls (PCBs), hexachlorobenzene (HCB), hexachlorocyclohexanes (HCHs), DDT and its metabolites (DDTs), chlordane compounds (CHLs), polybrominated diphenyl ethers (PBDEs), and methoxylated PBDEs (MeO-PBDEs). Analyses of stable isotopes δ13C and δ15N in skin resulted in further insight in their feeding ecology, which was in agreement with a diet focused mainly on low trophic level prey species, such as krill from Antarctica. POPs were measured in all humpback whales in the order of HCB > DDTs > CHLs > HCHs > PCBs > PBDEs > MeO-BDEs. HCB (median: 24 ng g−1 lw) and DDTs (median: 7.7 ng g−1 lw) were the predominant compounds in all whale biopsies. Among DDT compounds, p,p′-DDE was the major organohalogenated pollutant, reflecting its long-term accumulation in humpback whales. Significantly lower concentrations of HCB and DDTs were found in females than in males (p < 0.001). Other compounds were similar between the two genders (p > 0.05). Differences in the HCB and DDTs suggested gender-specific transfer of some compounds to the offspring. POP concentrations were lower than previously reported results for humpback whales sampled near the Antarctic Peninsula, suggesting potential influence of their nutritional status and may indicate different exposures of the whales according to their feeding zones. Further investigations are required to assess exposure of southern humpback whales throughout their feeding zones.
Show more [+] Less [-]Fin whales and microplastics: The Mediterranean Sea and the Sea of Cortez scenarios
2016
Fossi, Maria Cristina | Marsili, Letizia | Baini, Matteo | Giannetti, Matteo | Coppola, Daniele | Guerranti, Cristiana | Caliani, Ilaria | Minutoli, Roberta | Lauriano, Giancarlo | Finoia, Maria Grazia | Rubegni, Fabrizio | Panigada, Simone | Bérubé, Martine | Urbán Ramírez, Jorge | Panti, Cristina
The impact that microplastics have on baleen whales is a question that remains largely unexplored. This study examined the interaction between free-ranging fin whales (Balaenoptera physalus) and microplastics by comparing populations living in two semi-enclosed basins, the Mediterranean Sea and the Sea of Cortez (Gulf of California, Mexico). The results indicate that a considerable abundance of microplastics and plastic additives exists in the neustonic samples from Pelagos Sanctuary of the Mediterranean Sea, and that pelagic areas containing high densities of microplastics overlap with whale feeding grounds, suggesting that whales are exposed to microplastics during foraging; this was confirmed by the observation of a temporal increase in toxicological stress in whales. Given the abundance of microplastics in the Mediterranean environment, along with the high concentrations of Persistent Bioaccumulative and Toxic (PBT) chemicals, plastic additives and biomarker responses detected in the biopsies of Mediterranean whales as compared to those in whales inhabiting the Sea of Cortez, we believe that exposure to microplastics because of direct ingestion and consumption of contaminated prey poses a major threat to the health of fin whales in the Mediterranean Sea.
Show more [+] Less [-]Anthropogenic contaminants in Indo-Pacific humpback and Australian snubfin dolphins from the central and southern Great Barrier Reef
2013
Cagnazzi, Daniele | Fossi, Maria Cristina | Parra, Guido J. | Harrison, Peter L. | Maltese, Silvia | Coppola, Daniele | Soccodato, Alice | Bent, Michael | Marsili, Letizia
We present the first evidence of accumulation of organochlorine compounds (DDTs, PCBs, HCB) and polycyclic aromatic hydrocarbons (PAHs) in Indo-Pacific humpback and Australian snubfin dolphins from the central and southern Great Barrier Reef. These dolphins are considered by the Great Barrier Marine Park Authority to be high priority species for management. Analyses of biopsy samples, collected from free ranging individuals, showed PAHs levels comparable to those reported from highly industrialized countries. DDTs and HCB were found at low levels, while in some individuals, PCBs were above thresholds over which immunosuppression and reproductive anomalies occur. These results highlight the need for ongoing monitoring of these and other contaminants, and their potential adverse effects on dolphins and other marine fauna. This is particularly important given the current strategic assessment of the Great Barrier Reef World Heritage Area being undertaken by the Australian Government and the Queensland Government.
Show more [+] Less [-]Comparison of persistent organic pollutants (POPs) between small cetaceans in coastal and estuarine waters of the northern Gulf of Mexico
2019
Balmer, Brian | Ylitalo, Gina | Watwood, Stephanie | Quigley, Brian | Bolton, Jennie | Mullin, Keith | Rosel, Patricia | Rowles, Teri | Speakman, Todd | Wilcox, Lynsey | Zolman, Eric | Schwacke, Lorelei H.
Small cetaceans continue to be exposed to elevated levels of persistent organic pollutants (POPs). The goals of this study were to use data from remote biopsy sampling and photographic-identification to compare POP concentrations between small cetacean stocks in the northern Gulf of Mexico. During 2015–2017, 74 remote biopsies were collected in St. Andrew Bay and adjacent coastal waters from two species: common bottlenose dolphin (Tursiops truncatus) (N = 28, ♀; N = 42, ♂) and Atlantic spotted dolphin (Stenella frontalis) (N = 2, ♀; N = 2, ♂). Common bottlenose dolphin POP concentrations were significantly higher in St. Andrew Bay than coastal waters. Male St. Andrew Bay dolphins had the highest Σ DDT (dichlorodiphenyl-dichloroethane) levels measured in the southeastern U.S. (67 μg/g, 50–89 μg/g; geometric mean and 95% CI) and showed a significant negative relationship between Σ DDT and sighting distance from a St. Andrew Bay point source.
Show more [+] Less [-]Levels of arsenic, cadmium, lead and mercury in the branchial plate and muscle tissue of mobulid rays
2015
Ooi, Michelle S.M. | Townsend, Kathy A. | Bennett, Michael B. | Richardson, Anthony J. | Fernando, Daniel | Villa, Cesar A. | Gaus, Caroline
Mobulid rays are targeted in fisheries for their branchial plates, for use in Chinese medicine. Branchial plate and muscle tissue from Mobula japanica were collected from fish markets in Sri Lanka, and muscle tissue biopsies from Manta alfredi in Australia. These were analysed for arsenic, cadmium, lead and mercury and compared to maximum levels (MLs) set by Food Standards Australia and New Zealand (FSANZ), European Commission (EC) and Codex Alimentarius Commission. The estimated intake for a vulnerable human age group was compared to minimal risk levels set by the Agency for Toxic Substances and Disease Registry. The mean inorganic arsenic concentration in M. japanica muscle was equivalent to the FSANZ ML while cadmium exceeded the EC ML. The mean concentration of lead in M. alfredi muscle tissue exceeded EC and Codex MLs. There were significant positive linear correlations between branchial plate and muscle tissue concentrations for arsenic, cadmium and lead.
Show more [+] Less [-]Validating the use of biopsy sampling in contamination assessment studies of small cetaceans
2016
Méndez-Fernandez, Paula | Galluzzi Polesi, Paola | Taniguchi, Satie | de O. Santos, Marcos C. | Montone, Rosalinda C.
Remote biopsy sampling is the most common technique for acquiring samples from free-ranging marine mammals. However, such techniques may result in variable sampling being sometimes superficial skin and blubber biopsies. For decades, blubber has been used to monitor the exposure of marine mammals to persistent organic pollutants (POPs), but little is known regarding the variability of POPs as a function of blubber depth in small cetaceans and the available literature offers variable results. Thus, the aim of the present study was to validate biopsy sampling for monitoring contaminant concentrations in small, free-ranging cetaceans. Samples from the dorsal blubber of 10 incidentally captured Atlantic spotted dolphins (Stenella frontalis) were separated into two different layers (outer and inner) to investigate the influence of sampling depth on POP concentrations. POP concentrations were compared to those of the full blubber layer. The results revealed no significant differences in lipid content between males and females or among the inner, outer and full blubber layers (p>0.05). Moreover, the wet and lipid weight concentrations of all POP classes analysed [i.e. polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethanes (DDTs), polybrominated diphenyl ethers (PBDEs), hexachlorobenzene (HCB), hexachlorocyclohexanes (HCHs), chlordanes (CHLs) and mirex] did not differ significantly with blubber depth (p>0.05). POP classes followed the same decreasing order of wet weight concentrations in blubber layers and full blubber: PCBs>DDTs>PBDEs>mirex>HCB>HCHs>CHLs. Moreover, there was a low degree of differentiation in the accumulation of POP congeners. The present findings indicated that the distribution of contaminants was homogenous with blubber depth, which validates the use of biopsy sampling for the assessment of contaminants in small cetaceans.
Show more [+] Less [-]Use of skin and blubber tissues of small cetaceans to assess the trace element content of internal organs
2013
Aubail, A. | Méndez-Fernandez, P. | Bustamante, P. | Churlaud, C. | Ferreira, M. | Vingada, J.V. | Caurant, F.
In order to evaluate the use of biopsy samples as non-destructive tool for assessing trace element concentrations in small cetaceans, the concentrations of 14 trace elements were determined in skin, blubber, liver and kidneys of four species of small cetaceans (i.e. common dolphin Delphinus delphis, harbour porpoise Phocoena phocoena, bottlenose dolphin Tursiops truncatus and striped dolphin Stenella coeruleolba), stranded and/or by-caught along the NE Atlantic Ocean coast between 2001 and 2008. Only Cu, Fe, Hg, Mn, Ni and Zn were above the detection limit of the instruments and showed recoveries satisfactory enough to be interpreted. Among these trace elements, Hg was the only one showing a significant correlation between concentrations in and those in liver and kidneys. In consequence skin and blubber can only be used as non-invasive monitoring tissues to investigate Hg bioaccumulation in internal tissues for cetacean populations.
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