ABSTRACT
Common bottlenose dolphins serve as sentinels for the health of their coastal environments as they are susceptible to health impacts from anthropogenic inputs through both direct exposure and food web magnification. Remote biopsy samples have been widely used to reveal contaminant burdens in free-ranging bottlenose dolphins, but do not address the health consequences of this exposure. To gain insight into whether remote biopsies can also identify health impacts associated with contaminant burdens, we employed RNA sequencing (RNA-seq) to interrogate the transcriptomes of remote skin biopsies from 116 bottlenose dolphins from the northern Gulf of Mexico and southeastern U.S. Atlantic coasts. Gene expression was analyzed using principal component analysis, differential expression testing, and gene co-expression networks, and the results correlated to season, location, and contaminant burden. Season had a significant impact, with over 60% of genes differentially expressed between spring/summer and winter months. Geographic location exhibited lesser effects on the transcriptome, with 23.5% of genes differentially expressed between the northern Gulf of Mexico and the southeastern U.S. Atlantic locations. Despite a large overlap between the seasonal and geographical gene sets, the pathways altered in the observed gene expression profiles were somewhat distinct. Co-regulated gene modules and differential expression analysis both identified epidermal development and cellular architecture pathways to be expressed at lower levels in animals from the northern Gulf of Mexico. Although contaminant burdens measured were not significantly different between regions, some correlation with contaminant loads in individuals was observed among co-expressed gene modules, but these did not include classical detoxification pathways. Instead, this study identified other, possibly downstream pathways, including those involved in cellular architecture, immune response, and oxidative stress, that may prove to be contaminant responsive markers in bottlenose dolphin skin.
Subject(s)
Bottle-Nosed Dolphin/genetics , Environmental Exposure , Environmental Monitoring , Skin/metabolism , Transcriptome , Water Pollutants, Chemical/adverse effects , Animals , Female , Gulf of Mexico , Male , Sequence Analysis, RNA , South CarolinaABSTRACT
Common bottlenose dolphins (Tursiops truncatus), including those impacted by the 2010 Deepwater Horizon (DWH) oil spill, inhabit the coastal and estuarine waters of the northern Gulf of Mexico (GoM). In response to the spill, dolphin health assessments conducted in Barataria Bay, Louisiana - a site that experienced heavy and prolonged oiling - uncovered a high prevalence of health abnormalities and individuals in poor body condition. Although the health effects observed were suggestive of petroleum toxicity, a lack of pre-spill information regarding dolphin health raises the possibility that other environmental factors may have contributed to the adverse health of dolphins in this oil-impacted area. To assess how exposure to other environmental pollutants may affect the health of northern GoM dolphin populations impacted by the DWH oil spill, a suite of 69 persistent organic pollutants (POPs), including PCBs, PBDEs and organochlorine pesticides, was determined in blood and a subset of blubber samples collected during health assessments of 145 bottlenose dolphins at three GoM sites: two oil impacted sites - Barataria Bay, LA (BB), and Mississippi Sound, MS (MS) and an unimpacted reference site - Sarasota Bay, FL (SB). Overall, levels of POPs at all three sites appeared comparable or lower than concentrations previously reported for coastal bottlenose dolphin populations outside of the northern GoM. POP levels measured in BB dolphins were also comparable or lower than those measured at the unimpacted reference site (SB) within the northern GoM. Additionally, the relationship between blubber and blood contaminant levels in a smaller subset of BB and SB suggests that BB animals were not experiencing elevated blood-contaminant concentrations as a result of their poor body condition. Cumulatively, these results suggest that background levels of POPs measured are unlikely to produce the health abnormalities previously reported for BB dolphins.
Subject(s)
Adipose Tissue/chemistry , Bottle-Nosed Dolphin , Petroleum Pollution , Water Pollutants, Chemical/blood , Animals , Disasters , Environmental Monitoring , Gulf of Mexico , Louisiana , Mississippi , Water Pollutants, Chemical/analysisABSTRACT
As long-lived predators that integrate exposures across multiple trophic levels, cetaceans are recognized as sentinels for the health of marine ecosystems. Their utility as sentinels requires the establishment of baseline health parameters. Because cetaceans are protected, measurements obtained with minimal disruption to free ranging animals are highly desirable. In this study we investigated the utility of skin gene expression profiling to monitor health and contaminant exposure in common bottlenose dolphins (Tursiops truncatus). Remote integument biopsies were collected in the northern Gulf of Mexico prior to the Deepwater Horizon oil spill (May 2010) and during summer and winter for two years following oil contamination (2010-2011). A bottlenose dolphin microarray was used to characterize the skin transcriptomes of 94 individuals from three populations: Barataria Bay, Louisiana, Chandeleur Sound, Louisiana, and Mississippi Sound, Mississippi/Alabama. Skin transcriptomes did not differ significantly between populations. In contrast, season had a profound effect on gene expression, with nearly one-third of all genes on the array differing in expression between winter and the warmer seasons (moderated T-test; p<0.01, fold-change≥1.5). Persistent organic pollutants (POPs) in blubber changed concurrently, reaching >two-fold higher concentrations in summer compared to winter, due to a seasonal decrease in blubber thickness and loss of stored lipid. However, global gene expression did not correlate strongly with seasonally changing contaminant concentrations, most likely because the refractory, lipid-stored metabolites are not substrates for phase I or II xenobiotic detoxification pathways. Rather, processes related to cell proliferation, motility, and differentiation dominated the differences in expression in winter and the warmer seasons. More subtle differences were seen between spring and summer (1.5% of genes differentially expressed). However, two presumed oil-exposed animals from spring presented gene expression profiles more similar to the summer animals (presumed exposed) than to other spring animals. Seasonal effects have not previously been considered in studies assessing gene expression in cetaceans, but clearly must be taken into account when applying transcriptomic analyses to investigate their contaminant exposure or health status.
Subject(s)
Bottle-Nosed Dolphin/physiology , Seasons , Skin/metabolism , Transcriptome , Alabama , Animals , Biopsy , Climate , Cluster Analysis , Ecosystem , Female , Gene Expression Regulation , Geography , Gulf of Mexico , Louisiana , Male , Microarray Analysis , Mississippi , Nucleic Acid Hybridization , Petroleum Pollution/analysis , Principal Component Analysis , Water Pollutants, Chemical/analysis , XenobioticsABSTRACT
A number of studies were initiated in response to the Deepwater Horizon (DWH) oil spill to understand potential injuries to bottlenose dolphins (Tursiops truncatus) that inhabit the northern Gulf of Mexico (NGoM) estuarine waters. As part of these studies, remote biopsy skin and blubber samples were collected from dolphins at six field sites that received varying degrees of oiling: Barataria Bay (BB), Chandeleur Sound West (CSW), Chandeleur Sound East (CSE), Mississippi Sound South (MSS), Mississippi Sound North (MSN), and St. Joseph Bay (SJ). Blubber samples from 108 male dolphins were analyzed for persistent organic pollutant (POP) concentrations, as high levels of POPs have been previously reported in other southeastern U.S. dolphins and the potential contribution of these compounds to adverse health effects in NGoM dolphins must be considered. Dolphin blubber levels of summed POPs (ΣPOPs) did not differ significantly across sites (F-test, P=0.9119) [µg/g lipid; geometric mean and 95% CI]; CSW [65.9 (51.4-84.6)], SJ [74.1 (53.0-104)], MSN [74.3 (58.7-93.9)], BB [75.3 (56.4-101)], CSE [80.5 (57.8-112)], and MSS [82.5 (65.9-103)]. Overall, POP concentrations were in the lower half of the range compared to previously reported concentrations from other southeastern U.S. sites. Increased dolphin mortalities have been ongoing in the NGoM and have been suggested to be linked with the DWH oil spill. In addition, lung disease, impaired adrenal function, and serum biochemical abnormalities have been reported in dolphins from BB, an area that was heavily oiled. The results of this study suggest that POPs are likely not a primary contributor to the poor health conditions and increased mortality observed in some populations of NGoM dolphins following the DWH oil spill.
Subject(s)
Adipose Tissue/metabolism , Bottle-Nosed Dolphin/metabolism , Environmental Monitoring , Petroleum Pollution , Water Pollutants, Chemical/metabolism , Animals , Gulf of Mexico , Male , MississippiABSTRACT
We report concentrations of several classes of organochlorines (OCs) in the blubber of California sea lions (Zalophus californianus) from the Gulf of California. Summed OC levels measured in 34 wild-ranging animals were, in general, lower than those previously reported in sea lions from the eastern Pacific. The rank order of OCs was SigmaDDTs (mean=3400 ng g(-1 ) lipid weight [lw]) > SigmaPCBs (1400 ng g(-1 ) lw) > SigmaHCHs (50 ng g(-1 ) lw) >or= SigmaCHLORs (46 ng g(-1 ) lw). The most abundant OC measured was the DDT metabolite, p,p'-DDE. No significant differences in OC profiles were found between genders or rookeries. Although the mean concentrations of OCs measured in adult males and females were similar, only adult females had significantly higher (p<0.05) mean blubber concentrations of summation SigmaDDTs and summation SigmaHCHs than pups.