Modeling population effects of the Deepwater Horizon oil spill on a long-lived species.

The 2010 Deepwater Horizon (DWH) oil spill exposed common bottlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana to heavy oiling that caused increased mortality and chronic disease and impaired reproduction in surviving dolphins. We conducted photographic surveys and veterinary assessments in the decade following the spill. We assigned a prognostic score (good, fair, guarded, poor, or grave) for each dolphin to provide a single integrated indicator of overall health, and we examined temporal trends in prognostic scores. We used expert elicitation to quantify the implications of trends for the proportion of the dolphins that would recover within their lifetime. We integrated expert elicitation, along with other new information, in a population dynamics model to predict the effects of observed health trends on demography. We compared the resulting population trajectory with that predicted under baseline (no spill) conditions. Disease conditions persisted and have recently worsened in dolphins that were presumably exposed to DWH oil: 78% of those assessed in 2018 had a guarded, poor, or grave prognosis. Dolphins born after the spill were in better health. We estimated that the population declined by 45% (95% CI 14-74) relative to baseline and will take 35 years (95% CI 18-67) to recover to 95% of baseline numbers. The sum of annual differences between baseline and injured population sizes (i.e., the lost cetacean years) was 30,993 (95% CI 6607-94,148). The population is currently at a minimum point in its recovery trajectory and is vulnerable to emerging threats, including planned ecosystem restoration efforts that are likely to be detrimental to the dolphins' survival. Our modeling framework demonstrates an approach for integrating different sources and types of data, highlights the utility of expert elicitation for indeterminable input parameters, and emphasizes the importance of considering and monitoring long-term health of long-lived species subject to environmental disasters. Article impact statement: Oil spills can have long-term consequences for the health of long-lived species; thus, effective restoration and monitoring are needed.

El derrame de petróleo Deepwater Horizon (DWH) en 2010 expuso gravemente a este hidrocarburo a los delfines (Tursiops truncatus) de la Bahía Barataria, Luisiana, causando un incremento en la mortalidad y en las enfermedades crónicas, y deteriorando la reproducción de los delfines sobrevivientes. Realizamos censos fotográficos y evaluaciones veterinarias durante la década posterior al derrame. Asignamos un puntaje pronóstico (bueno, favorable, moderado, malo, o grave) a cada delfín para proporcionar un indicador integrado único de la salud en general. También examinamos las tendencias temporales de estos puntajes. Usamos información de expertos para cuantificar las implicaciones de las tendencias para la proporción de delfines que se recuperaría dentro de su periodo de vida. Integramos esta información, junto con información nueva, a un modelo de dinámica poblacional para predecir los efectos sobre la demografía de las tendencias observadas en la salud. Comparamos la trayectoria poblacional resultante con aquella pronosticada bajo condiciones de línea base (sin derrame). Las condiciones de enfermedad persistieron y recientemente han empeorado en los delfines que supuestamente estuvieron expuestos al petróleo de DWH: 78% de aquellos evaluados en 2018 tuvieron un pronóstico moderado, malo o grave. Los delfines que nacieron después del derrame contaron con mejor salud. Estimamos que la población declinó en un 45% (95% CI 14-74) relativo a la línea base y tardará 35 años (95% CI 18-67) en recuperar el 95% de los números de línea base. La suma de las diferencias anuales entre el tamaño poblacional de línea base y el dañado (es decir, los años cetáceos perdidos) fue de 30,993 (95% CI 6,607-94,148). La población actualmente está en un punto mínimo de su trayectoria de recuperación y es vulnerable a las amenazas emergentes, incluyendo los esfuerzos de restauración ambiental planeada que probablemente sean nocivos para la supervivencia de los delfines. Nuestro marco de modelado demuestra una estrategia para la integración de diferentes fuentes y tipos de datos, resalta la utilidad de la información de expertos para los parámetros de aportación indeterminable, y enfatiza la importancia de la consideración y el monitoreo de la salud a largo plazo de las especies longevas sujetas a los desastres ambientales. Modelado de los Efectos Poblacionales del Derrame de Petróleo Deepwater Horizon sobre Especies Longevas.

Cardiac assessments of bottlenose dolphins (Tursiops truncatus) in the Northern Gulf of Mexico following exposure to Deepwater Horizon oil.

The Deepwater Horizon (DWH) oil spill profoundly impacted the health of bottlenose dolphins (Tursiops truncatus) in Barataria Bay, LA (BB). To comprehensively assess the cardiac health of dolphins living within the DWH oil spill footprint, techniques for in-water cardiac evaluation were refined with dolphins cared for by the U.S. Navy Marine Mammal Program in 2018 and applied to free-ranging bottlenose dolphins in BB (n = 34) and Sarasota Bay, Florida (SB) (n = 19), a non-oiled reference population. Cardiac auscultation detected systolic murmurs in the majority of dolphins from both sites (88% BB, 89% SB) and echocardiography showed most of the murmurs were innocent flow murmurs attributed to elevated blood flow velocity [1]. Telemetric six-lead electrocardiography detected arrhythmias in BB dolphins (43%) and SB dolphins (31%), all of which were considered low to moderate risk for adverse cardiac events. Echocardiography showed BB dolphins had thinner left ventricular walls, with significant differences in intraventricular septum thickness at the end of diastole (p = 0.002), and left ventricular posterior wall thickness at the end of diastole (p = 0.033). BB dolphins also had smaller left atrial size (p = 0.004), higher prevalence of tricuspid valve prolapse (p = 0.003), higher prevalence of tricuspid valve thickening (p = 0.033), and higher prevalence of aortic valve thickening (p = 0.008). Two dolphins in BB were diagnosed with pulmonary arterial hypertension based on Doppler echocardiography-derived estimates and supporting echocardiographic findings. Histopathology of dolphins who stranded within the DWH oil spill footprint showed a significantly higher prevalence of myocardial fibrosis (p = 0.003), regardless of age, compared to dolphins outside the oil spill footprint. In conclusion, there were substantial cardiac abnormalities identified in BB dolphins which may be related to DWH oil exposure, however, future work is needed to rule out other hypotheses and further elucidate the connection between oil exposure, pulmonary disease, and the observed cardiac abnormalities.

Blubber steroid hormone profiles as indicators of physiological state in free-ranging common bottlenose dolphins (Tursiops truncatus).

Blubber has been proposed as a possible alternative to blood in the assessment of endocrine physiology in marine mammals because it can be collected via remote biopsy, which removes some of the confounding variables and logistical constraints associated with blood collection. To date, few studies have directly assessed the relationships between circulating versus blubber steroid hormone profiles in marine mammals, and these studies have been limited to a small subset of steroid hormones, which collectively limit the current utility of blubber steroid hormone measurements. In this study, we used liquid-chromatography tandem-mass spectrometry (LC-MS/MS) to screen for 16 steroid hormones in matched blood and blubber samples from free-ranging common bottlenose dolphins (Tursiops truncatus). Seven steroid hormones were detected and quantified, including two progestogens, two androgens, and three corticosteroids. Using principal components analysis (PCA), we explored relationships between hormones in both matrices and three physiological states: sexual maturity, pregnancy, and acute stress response. Plasma and blubber testosterone and its precursors, 17-hydroxyprogesterone and androstenedione, loaded to the first principal component (PC1), and PC1 scores were higher in mature males. Plasma and blubber progesterone loaded to PC2, and pregnant/probable pregnant females had significantly higher PC2 scores. Pregnant females also had higher PC1 scores than other females, suggesting differences in androgen profiles between these groups. There was disagreement between plasma and blubber corticosteroid profiles, as indicated by their loading to different PCs; plasma corticosteroids loaded to PC3 and blubber corticosteroids to PC4. PC3 scores were significantly predicted by elapsed time to blood collection (i.e., time between initiating the capture process and blood collection), while elapsed time to blubber collection significantly predicted PC4 scores, indicating that corticosteroid profiles shift in both tissues during acute stress. Corticosteroid profiles were not related to demographic group, site-month, body mass index, water temperature, or time spent outside of the water on the processing boat. Overall, these results demonstrate that blubber steroid hormone profiles reflect changes in endocrine function that occur over broad temporal scales.

Remote blubber sampling paired with liquid chromatography tandem mass spectrometry for steroidal endocrinology in free-ranging bottlenose dolphins (Tursiops truncatus).

Liquid chromatography tandem mass spectrometry allows for the measurement of steroid hormone suites in the blubber of marine mammals. By combining this technology with minimally invasive techniques such as remote biopsy, endocrine profiles can be assessed, allowing for studies of hormonal profile variation over time. In this study, we explored associations among different steroidogenic pathways and seasonal differences in blubber hormone profiles of free-ranging common bottlenose dolphins along the coast of South Carolina, USA. Male dolphins experience a peak in testosterone, androstenedione, progesterone, and 17-hydroxyprogesterone in the spring, likely related to an upregulation of the androgen steroidogenic pathway during mating season. We also observed increased cortisol concentrations during summer compared to winter. Among females, there was an increase in androstenedione with elevated progesterone concentrations indicative of pregnancy, highlighting another potential endocrine marker for pregnancy in free-ranging dolphins. This work emphasizes the importance of selecting the appropriate season for studies on endocrine status to effectively uncover physiological variation or disruption in free-ranging cetaceans.

Skin Transcriptomes of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico and southeastern U.S. Atlantic coasts.

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.

Persistent organic pollutants (POPs) in blood and blubber of common bottlenose dolphins (Tursiops truncatus) at three northern Gulf of Mexico sites following the Deepwater Horizon oil spill.

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.

Density, abundance, survival, and ranging patterns of common bottlenose dolphins (Tursiops truncatus) in Mississippi Sound following the Deepwater Horizon oil spill.

After the Deepwater Horizon (DWH) oil spill began in April 2010, studies were initiated on northern Gulf of Mexico common bottlenose dolphins (Tursiops truncatus) in Mississippi Sound (MSS) to determine density, abundance, and survival, during and after the oil spill, and to compare these results to previous research in this region. Seasonal boat-based photo-identification surveys (2010-2012) were conducted in a section of MSS to estimate dolphin density and survival, and satellite-linked telemetry (2013) was used to determine ranging patterns. Telemetry suggested two different ranging patterns in MSS: (1) inshore waters with seasonal movements into mid-MSS, and (2) around the barrier islands exclusively. Based upon these data, dolphin density was estimated in two strata (Inshore and Island) using a spatially-explicit robust-design capture-recapture model. Inshore and Island density varied between 0.77-1.61 dolphins km-2 ([Formula: see text] = 1.42, 95% CI: 1.28-1.53) and 3.32-5.74 dolphins km-2 ([Formula: see text] = 4.43, 95% CI: 2.70-5.63), respectively. The estimated annual survival rate for dolphins with distinctive fins was very low in the year following the spill, 0.73 (95% CI: 0.67-0.78), and consistent with the occurrence of a large scale cetacean unusual mortality event that was in part attributed to the DWH oil spill. Fluctuations in density were not as large or seasonally consistent as previously reported. Total abundance for MSS extrapolated from density results ranged from 4,610 in July 2011 to 3,046 in January 2012 ([Formula: see text] = 3,469, 95% CI: 3,113-3,725).

Reproductive outcome and survival of common bottlenose dolphins sampled in Barataria Bay, Louisiana, USA, following the Deepwater Horizon oil spill.

Common bottlenose dolphins (Tursiops truncatus) inhabit bays, sounds and estuaries across the Gulf of Mexico. Following the Deepwater Horizon oil spill, studies were initiated to assess potential effects on these ecologically important apex predators. A previous study reported disease conditions, including lung disease and impaired stress response, for 32 dolphins that were temporarily captured and given health assessments in Barataria Bay, Louisiana, USA. Ten of the sampled dolphins were determined to be pregnant, with expected due dates the following spring or summer. Here, we report findings after 47 months of follow-up monitoring of those sampled dolphins. Only 20% (95% CI: 2.50-55.6%) of the pregnant dolphins produced viable calves, as compared with a previously reported pregnancy success rate of 83% in a reference population. Fifty-seven per cent of pregnant females that did not successfully produce a calf had been previously diagnosed with moderate-severe lung disease. In addition, the estimated annual survival rate of the sampled cohort was low (86.8%, 95% CI: 80.0-92.7%) as compared with survival rates of 95.1% and 96.2% from two other previously studied bottlenose dolphin populations. Our findings confirm low reproductive success and high mortality in dolphins from a heavily oiled estuary when compared with other populations. Follow-up studies are needed to better understand the potential recovery of dolphins in Barataria Bay and, by extension, other Gulf coastal regions impacted by the spill.

Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico.

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.

Persistent organic pollutants (POPs) in blubber of common bottlenose dolphins (Tursiops truncatus) along the northern Gulf of Mexico coast, USA.

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.

Health of common bottlenose dolphins ( Tursiops truncatus ) in Barataria Bay, Louisiana, following the deepwater horizon oil spill.

The oil spill resulting from the explosion of the Deepwater Horizon drilling platform initiated immediate concern for marine wildlife, including common bottlenose dolphins in sensitive coastal habitats. To evaluate potential sublethal effects on dolphins, health assessments were conducted in Barataria Bay, Louisiana, an area that received heavy and prolonged oiling, and in a reference site, Sarasota Bay, Florida, where oil was not observed. Dolphins were temporarily captured, received a veterinary examination, and were then released. Dolphins sampled in Barataria Bay showed evidence of hypoadrenocorticism, consistent with adrenal toxicity as previously reported for laboratory mammals exposed to oil. Barataria Bay dolphins were 5 times more likely to have moderate-severe lung disease, generally characterized by significant alveolar interstitial syndrome, lung masses, and pulmonary consolidation. Of 29 dolphins evaluated from Barataria Bay, 48% were given a guarded or worse prognosis, and 17% were considered poor or grave, indicating that they were not expected to survive. Disease conditions in Barataria Bay dolphins were significantly greater in prevalence and severity than those in Sarasota Bay dolphins, as well as those previously reported in other wild dolphin populations. Many disease conditions observed in Barataria Bay dolphins are uncommon but consistent with petroleum hydrocarbon exposure and toxicity.

Evaluation and comparison of the health status of Atlantic bottlenose dolphins from the Indian River Lagoon, Florida, and Charleston, South Carolina.

OBJECTIVE: To conduct health assessments and compare outcomes in 2 populations of Atlantic bottlenose dolphins. Design-Repeated cross-sectional study. ANIMALS: 171 Atlantic bottlenose dolphins. PROCEDURES: During June and August of 2003 through 2005, 89 dolphins from the Indian River Lagoon (IRL), Florida, and 82 dolphins from estuarine waters near Charleston, SC, were evaluated. A panel of 5 marine mammal veterinarians classified dolphins as clinically normal, possibly diseased, or definitely diseased on the basis of results of physical and ultrasonographic examinations, hematologic and serum biochemical analyses, and cytologic and microbiologic evaluations of gastric contents and swab specimens. RESULTS: Prevalence of dolphins classified as definitely diseased did not differ significantly between the IRL (32%) and Charleston (20%) sites. Proportions of dolphins classified as possibly diseased also did not differ. Lobomycosis was diagnosed in 9 dolphins from the IRL but in none of the dolphins from Charleston. Proportions of dolphins with orogenital papillomas did not differ significantly between the IRL (12%) and Charleston (7%) sites. From 2003 through 2005, the proportion classified as definitely diseased tripled among dolphins from the Charleston site but did not increase significantly among dolphins from the IRL. Dolphins from the Charleston site were more likely to have leukocytosis, lymphocytosis, and low serum concentrations of total protein and total J-globulins than were dolphins from the IRL. CONCLUSIONS AND CLINICAL RELEVANCE: High prevalences of diseased dolphins were identified at both sites; however, the host or environmental factors that contributed to the various abnormalities detected are unknown.

Geographic variation in polychorinated biphenyl and organochlorine pesticide concentrations in the blubber of bottlenose dolphins from the US Atlantic coast.

Concentrations of polychorinated biphenyls (PCBs) and other organochlorine contaminants (OCs) were measured in blubber collected from live bottlenose dolphins (Tursiops truncatus) at three sites along the United States Atlantic coast. Dolphins were sampled via surgical biopsy during capture-release studies near Charleston, South Carolina and Beaufort, North Carolina. Additional animals were sampled using remote biopsy techniques in estuarine waters near Charleston and from the Indian River Lagoon, Florida. Overall concentrations of major contaminant groups were found to vary between sites and mean concentrations of most OCs from male dolphins in the Indian River Lagoon were less than half of those measured from Charleston and Beaufort males. Geometric mean total PCB concentrations were 30, 27 and 14 microg/g lipid for male dolphins sampled in Beaufort, Charleston and the Indian River Lagoon, respectively. Significant variation related to sex- and age-class, as well as geographic sampling location, was seen in the PCB congener profiles. The measured PCB concentrations, although lower than those reported for stranded animals from the 1987/1988 epizootic along the United States mid-Atlantic coast, are sufficiently high to warrant concern for the health of dolphins from the sampled populations, particularly the animals near Charleston and Beaufort.