In April 2010, the Deepwater Horizon (DWH) offshore drilling rig exploded and sank, resulting in large-scale release of oil that contaminated bays, sounds, and estuaries in the northern Gulf of Mexico (NGoM) (Michel et al., 2013). More than 3 million barrels of oil (~900 million pounds) were released before the well was sealed (U.S. v. BP et al., 2015), resulting in an oil slick that spanned ~43,000 square miles of water and oiled more than 1,000 miles of shoreline habitats (Michel et al., 2013; ERMA, 2015). Although clean-up efforts removed ~600 million pounds of oil-contaminated waste from Gulf waters and nearshore habitats of the NGoM (EPA, 2011), the oil spill caused substantial injury to marine life (Deepwater Horizon Natural Resource Damage Assessment (NRDA) Trustees, 2016).

As DWH oil spread throughout the NGoM, multiple cetacean species were observed in the oiled areas (Aichinger Dias et al., 2017). Response monitoring activities from April through September 2010 documented more than 1,100 individuals of 10 different cetacean species swimming through thick surface oil or surface oil sheen ( Figure 1 ) (Aichinger Dias et al., 2017; Wilkin et al., 2017). Cetaceans living within the oil spill footprint were likely exposed through multiple routes, including inhalation of volatile organic compounds, direct aspiration of oil droplets, ingestion with or without subsequent aspiration, and dermal absorption of oil and its toxic components (Takeshita et al., 2017). Further, oral ingestion may have occurred through incidental ingestion of oil on the surface of the water and/or suspended in the water column, or through the ingestion of contaminated prey and/or sediments during foraging activities (Godard-Codding and Collier, 2018; Quigley et al., 2022).

In the months that followed, one of the largest and longest-lasting marine mammal Unusual Mortality Events (UMEs) documented in the NGoM began and continued through 2014 (Litz et al., 2014). Marine mammal stranding network responders collected biological data and samples from carcasses, and after a comprehensive investigation into all potential causes of the mortality event, the most likely cause was determined to be the DWH oil spill (Venn-Watson et al., 2015a). Some of the most consistent necropsy findings within the oil spill footprint were bronchopneumonia and adrenal gland atrophy in non-perinate dolphins and an increased prevalence of fetal distress and in utero pneumonia in dead perinates (Venn-Watson et al., 2015b; Colegrove et al., 2016).

While the marine mammal UME investigation was underway, a Natural Resource Damage Assessment (NRDA) was being conducted to assess the potential impact of the DWH oil spill on the NGoM ecosystem, including marine mammals. Live bottlenose dolphins (Tursiops truncatus) living in heavily-oiled Barataria Bay (BB), Louisiana, and oil-impacted Mississippi Sound (MS), Mississippi/Alabama, received comprehensive health exams during catch-and-release field studies. Live dolphins were also examined in Sarasota Bay (SB), Florida, a comparison site with no DWH oil contamination. Dolphins in the heavily-oiled sites had multiple health issues, including moderate to severe lung disease, poor body condition, an impaired stress response, and hematological/serum chemistry indicators of inflammation, hypoglycemia, and abnormal iron levels (Schwacke et al., 2014). During 2011-2013, nearly half of the dolphins evaluated by experienced marine mammal veterinarians in oil-impacted habitats (BB and MS) were considered unhealthy, indicated by a guarded or worse prognosis, and 17% percent of examined dolphins received a poor or grave prognosis, meaning they were not expected to survive (Schwacke et al., 2014).

The increased prevalence of dolphins with compromised health coincided with high mortality rates within the oil spill footprint. Follow-up studies of BB dolphins using mark-recapture survival models yielded estimated annual mortality rates of 13.2-19.6% in the years immediately following the spill (Lane et al., 2015; McDonald et al., 2017), which were much higher than mortality rates previously reported for bottlenose dolphins using similar techniques near Charleston, South Carolina (4.9%), and Sarasota, Florida (3.8%) (Wells and Scott, 1990; Speakman et al., 2010). Alternative hypotheses were considered, including exposure to harmful algal blooms (Deepwater Horizon Natural Resource Damage Assessment (NRDA) Trustees, 2016), persistent organic pollutants (Balmer et al., 2015), and infectious disease outbreaks (Venn-Watson et al., 2015a). These factors were ruled out as likely contributors to the increased mortality rates, and exposure to toxic oil components was determined to be the most likely cause of increased mortality within the DWH oil spill footprint (Deepwater Horizon Natural Resource Damage Assessment (NRDA) Trustees, 2016; Takeshita et al., 2017).

In the year following the DWH spill, dolphins examined within the oil spill footprint had an approximately 5-fold higher prevalence of moderate to severe lung disease compared to dolphins living outside the oiled region, based on pulmonary ultrasound examination (0.34 in BB versus 0.07 in SB, the comparison site) (Schwacke et al., 2014). During 2013 and 2014, the prevalence of moderate to severe lung disease among BB dolphins decreased slightly (0.23 and 0.25, respectively), but remained elevated relative to the prevalence at the SB non-oiled comparison site (Smith et al., 2017). Concurrent pathology investigations of dead dolphins recovered from the NGoM in the years following the spill documented similar pulmonary findings (Venn-Watson et al., 2015b). The prevalence of bacterial pneumonias, many severe, in carcasses recovered within the oil spill footprint was significantly higher than in comparison populations [0.22 (oiled) vs 0.02 (non-oiled)]. Pneumonias were caused by multiple bacterial pathogens, indicating that lung disease was not due to infection with a single, highly pathogenic bacterium, and may have been due to secondary infection of damaged lung tissue (Venn-Watson et al., 2015b).

The increased prevalence of lung disease in dolphins living within the DWH oil spill footprint was consistent with respiratory findings from humans exposed to oil and its toxic components (Zock et al., 2007; Jung et al., 2013; Alexander et al., 2018; Gam et al., 2018a; Gam et al., 2018b). However, relatively few studies have focused on the chronicity of respiratory disease post-exposure (Zock et al., 2012; Zock et al., 2014; Lawrence et al., 2020). Here we combined these previously reported data with additional data collected from 2016-2018 as part of a Gulf of Mexico Research Initiative study to examine temporal trends and assess if pulmonary disease persisted in wild dolphins as a chronic effect of the DWH oil spill.

Between 2011 and 2018, we evaluated the pulmonary health of 171 BB dolphins: 132 were alive at the time of the spill (2010) and 18 were born post-spill. Age cohort classification could not be determined for 21 BB individuals. Over the same time period, we assessed the pulmonary health of 103 dolphins from the unoiled comparison site (SB): 85 were alive at the time of the spill (2010) and 18 were born post-spill.

In the aftermath of the DWH disaster and subsequent oiling of estuarine and coastal habitats, a high prevalence of moderate to severe lung disease was found in bottlenose dolphins living within Barataria Bay, one of the heaviest oiled estuaries. BB dolphins have high site fidelity, meaning that animals tend to live in the same region for multiple years and are unlikely to leave (Lane et al., 2015; Wells et al., 2017). Our results determined that dolphin pulmonary health has not improved for BB dolphins alive during the spill. The high prevalence of moderate to severe lung disease years following the spill suggests that the lung damage that occurred is chronic and likely progressive, which should be considered when investigating potential pathways and mechanisms of respiratory compromise. Other conditions that possibly contributed to the chronic lung disease included an increased susceptibility to lung infections due to oil-induced immune system aberrations (De Guise et al., 2021), cardiac damage with secondary pulmonary compromise (Linnehan et al., 2021), and/or age-related health changes.

In bottlenose dolphins and other cetaceans, the lungs serve a dual purpose of both respiration and buoyancy control (Ridgway et al., 1969). Investigations of dolphin pulmonary anatomy have shown that terminal airways are reinforced with cartilage, and myoelastic sphincters surround terminal bronchioles and alveolar entrances (Simpson & Gardner, 1972). The alveoli can completely collapse at depth, forcing air into the reinforced air spaces, presumably for prevention of decompression sickness (Ridgway et al., 1969). The presence of moderate to severe pulmonary disease would be expected to impair these physiologic mechanisms, negatively impact buoyancy, and increase energetic demands. This is supported by the authors’ (CRS, FMG, FIT, JMM, MI, RSW) personal observations of dolphins in human care diagnosed with moderate to severe pulmonary disease that have altered swim and dive patterns, likely due to decreased functional lung capacity and concomitant impaired buoyancy.

The physiological adaptions of dolphin lungs that support diving and swimming in marine ecosystems may make these species more susceptible than humans and other air-breathing animals to the negative impacts associated with inhaled or aspirated contaminants. Cetaceans breathe at the air-water interface, where high levels of volatile compounds and oil-containing aerosols and droplets were released from the DWH oil slick (de Gouw et al., 2011; Ryerson et al., 2012). Adult bottlenose dolphins take rapid breaths that begin with an explosive exhalation and are followed by deep inhalation of ~10 liters of surrounding air into their lungs, all in less than a second (Ridgway et al., 1969; Piscitelli et al., 2013). This air intake goes directly from the blowhole to the dolphin’s lungs, without protective cilia or nasal turbinates to filter the air. Dolphins often hold their breath for several minutes while swimming, foraging, and interacting with others, before returning to the surface of the water to take several breaths. During these respiratory cycles, dolphins exchange up to 90% of deep lung air (Ridgway et al., 1969), which could allow contaminants ample time and opportunity to impact the lung tissue.

A potential route of oil exposure in marine mammals is aspiration of liquid oil from the surface of the water and/or aerosolized oil droplets (Takeshita et al., 2017). During the DWH oil spill event, dolphins were seen surfacing in oil slicks and others were documented with crude oil on their heads ( Figure 1 ) (Schwacke et al., 2014). In animals, aspiration of petroleum products (e.g. kerosene, crude oil) can cause direct injury to lung tissue or lead to aspiration pneumonia (Coppock et al., 2012; Mostrom, 2021). In dolphins, active infectious pneumonia of varying severity has been well documented (Smith et al., 2012). Less frequently, aspiration pneumonia has been diagnosed and managed (CRS, FMG, JMM unpublished). For animals in human care, clinical evidence typically includes elevated blood-based markers of systemic inflammation, confirmation of pneumonia on radiography and/or computed tomography, isolation of infectious agents from respiratory tract sampling, and a positive response to therapy. When treatment is effective, complete or near-complete resolution of the pulmonary abnormalities can occur. In wild dolphins with no access to medical treatment, aspiration pneumonia could be fatal, and if survived, could plausibly lead to chronic, pulmonary disease.

Moderate to severe AIS remains a persistent finding in BB dolphins (2011-2018). Possible causes include pneumonia, pulmonary edema, and pulmonary fibrosis (Smith et al., 2012). During the initial health assessments of BB dolphins (2011), infectious pneumonia was considered the most likely cause of AIS based on associated ultrasound findings (such as consolidation) and blood-based evidence of inflammation, anemia, and possible septicemia (Schwacke et al., 2014). In subsequent years (2013-2014), the animals’ overall health status stabilized somewhat, and chronic, pulmonary diseases were considered more likely than active, infectious pneumonias (Smith et al., 2017). From 2016-2018, the clinical picture slightly deteriorated, with increasing prevalence of severe lung disease. Several of the BB dolphins had a pattern of AIS that was more severe ventrally than dorsally (2016-2018).

This AIS pattern has been previously reported in three cetaceans with pulmonary edema; two geriatric bottlenose dolphins with congestive heart failure (Smith et al., 2012) and one mature vaquita porpoise (Phocoena sinus) that developed pulmonary edema secondary to capture myopathy (Rojas-Bracho et al., 2019). However, we considered pulmonary edema unlikely in most BB dolphin cases given the lack of additional clinical findings to support this diagnosis. Although a concurrent cardiac health study showed a higher prevalence of heart chamber abnormalities in BB dolphins than SB dolphins (e.g. thinner left ventricular walls, smaller left atria, tricuspid valve prolapse and thickening, aortic valve thickening) as diagnosed with echocardiography (Linnehan et al., 2021), the cardiac abnormalities in most animals were not considered significant enough to cause clinical manifestations. Additional data would be needed to determine if low-grade underlying cardiac abnormalities could lead to secondary pulmonary edema, specifically under brief capture conditions.

Chronic, progressive pulmonary fibrosis was also considered as a potential explanation for the AIS seen in BB dolphins. Pulmonary fibrosis occurs as a consequence of significant lung injury and is associated with scarring that can progress over time and eventually lead to death. There are numerous types and causes of pulmonary fibrosis, including etiologies related to environmental exposure to chemicals and pathogens (Huang and Tang, 2021; Vlahovich and Sood, 2021; Moss et al., 2022). Although pulmonary fibrosis hasn’t been definitely diagnosed with ultrasound in dolphins, ultrasound findings have been described in human patients. These include pleural thickening, pleural irregularity, and an increase in B-line (or ring-down) artifacts that can coalesce with severity to create a ‘white out’ appearance (Manolescu et al., 2018). Although pleural thickness measurements have not been standardized in dolphins, we subjectively noted thickened and irregular pleura in the majority of BB dolphins, more severe ventrally than dorsally, and dolphins with severe AIS had a characteristic ‘white-out’ appearance to the lung. Therefore, it is reasonable that at least some of the BB dolphins examined had pulmonary fibrosis. Even so, there is still no clear explanation for why the fibrosis would worsen ventrally, unless it reflected a gravity-dependent inhalation pattern or previous aspiration injury within the lungs that progressed over time.

Pulmonary angiomatosis has been observed in stranded Gulf of Mexico dolphins and can cause interstitial and pleural thickening, often increasing with age (Venn-Watson et al., 2015b). While the potential contribution of underlying pulmonary angiomatosis to AIS needs to be further examined, there are no current data to support that angiomatosis worsens ventrally in the lung, or would be more prevalent in BB versus SB dolphins. A critical need exists to collect and study the carcasses of BB dolphins. Histopathologic analysis of their lung tissue could help determine if chronic progressive pulmonary fibrosis, or another pulmonary interstitial disease, has emerged as a health issue in BB dolphins as a consequence of the DWH oil spill.

Pulmonary damage and subsequent respiratory compromise are not unusual findings several years after exposure to an oil spill. Respiratory symptoms following inhalation exposure from various spills were reported in humans, including the DWH disaster (Alexander et al., 2018; Rusiecki et al., 2018). Experimental studies involving fish and mice exposed to DWH oil and/or associated chemicals reported respiratory injury (Brown-Peterson et al., 2015; Jaligama et al., 2015; Pan et al., 2018). Potential mechanisms of primary injury have been compared across taxa, including oxidative damage, cellular damage, and cellular necrosis (Takeshita et al., 2021). Secondary pathways have also been investigated, including immunotoxicity, cardiotoxicity, and chronic stress.

Based on the comprehensive examination of all available data collected to date, chronic pulmonary disease was likely a significant factor in the overall poor health of dolphins living within the DWH oil spill footprint. There were additional consequences to dolphins that sustained this injury. To help define clinical significance to individual animals, oxygenation and blood gas analyses were conducted (2016 and 2017), which identified evidence of compensatory acid-base disturbances in dolphins with lung disease (Sharp et al., 2017). Poor pulmonary health and acid-base imbalances could contribute to the sustained high rates of dolphin reproductive failure in BB dolphins (Lane et al., 2015; Kellar et al., 2016; Smith et al., 2020), as maternal illness and related adverse health outcomes could put pregnancies at risk and impact a female dolphin’s ability to adequately care for her calf. Additionally, overall health scores in BB dolphins showed that dolphin population health has not improved over time (2011-2018) and in some cases has worsened (Schwacke et al., 2022).

A slight increase in prevalence of moderate lung disease was seen in pre-spill SB dolphins (comparison site) sampled during 2016 and 2017. Sample size for this cohort was very limited (5 in 2016; 8 in 2017), so caution is warranted when interpreting these findings. Furthermore, there were no documented cases of pulmonary masses, pulmonary consolidation, or ventrally severe AIS in SB during 2017 or 2018. Additionally, no cases of severe pulmonary disease were diagnosed in SB during the entire post-DWH disaster study period, compared to a prevalence of 0.23 in 2017 and 0.22 in 2018 in oiled BB.

Dolphins born after the DWH oil spill did not have an elevated prevalence of pulmonary disease. In fact, the prevalence of moderate to severe lung disease in BB dolphins born post-spill was similar to SB dolphins not impacted by the DWH oil spill, which is an encouraging finding for this generation of BB dolphins. Although these animals were relatively young at the time of exam (<10 years old), our previous study showed that age was not a significant factor in the prevalence of moderate to severe lung disease in BB dolphins (Smith et al., 2017). Additional monitoring studies will be needed to determine if the prevalence of lung disease in dolphins born post-spill remains similar to SB over time.

This study showed strong evidence of chronic and potentially progressive respiratory injury in bottlenose dolphins living within the DWH oil spill footprint. Other cetacean species living farther off-shore were also exposed, but their health was difficult to evaluate and few data exist to determine the potential adverse health impacts. However, the nearshore bottlenose dolphin data suggests that any cetacean with a similar exposure to DWH oil or its byproducts could sustain a similar injury. Long-term monitoring of dolphin populations living within the oil spill footprint is critical to fully understand the potential for and timeline of individual and population recovery from the impacts of a such a large-scale oil spill event, and to extrapolate impacts on other cetacean populations in the NGoM and elsewhere. As long-lived, air-breathing mammals that live, feed, and breed along the coastline, dolphins can be considered a sentinel species and provide valuable insight into the chronic effects of oil and associated contaminants on animal, human, and ecosystem health.

Data are publicly available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (doi: 10.7266/N7H41PTV, 10.7266/n7-76aj-rp39, 10.7266/n7-sv57-1h12).

The animal study was reviewed and approved by National Marine Fisheries Service’s Institutional Animal Care and Use Committee and Mote Marine Laboratory’s Institutional Animal Care and Use Committee.

CS: conceptualization, methodology, formal analysis, investigation, writing – original draft, visualization, supervision, project administration, funding acquisition. TR: conceptualization, methodology, writing – review and editing, supervision, resources, project administration, funding acquisition. FG: investigation, formal analysis, writing – review and editing, supervision, project administration, funding acquisition. MI: investigation, formal analysis, writing – review and editing, funding acquisition. KC: investigation, formal analysis, writing – review and editing. RT: formal analysis, data curation, validation, writing – review and editing. FT: investigation, writing – review and editing. EZ: investigation, writing – review and editing. JM: data curation, synthesis, and analysis, writing – review and editing. VC: investigation, writing – review and editing. JM: investigation, writing – review and editing. WM: investigation, data synthesis, writing – review and editing. TS: investigation, writing – review and editing. AB: data synthesis, writing – review and editing. RW: investigation, writing – review and editing, resources, funding acquisition. LS: conceptualization, methodology, statistical analysis, validation, writing – review and editing, visualization, project administration, funding acquisition. All authors contributed to the article and approved the submitted version.

This research was made possible in part by a grant from The Gulf of Mexico Research Initiative (Award SA16-17), and as part of the Deepwater Horizon Natural Resource Damage Assessment. We appreciate the efforts of numerous organizations and their researchers, veterinarians, technicians, students, and volunteers who provided support for the health assessment projects, which include our home institutions as well as the Audubon Nature Institute, Dolphin Quest, International Fund for Animal Welfare, Louisiana Department of Wildlife and Fisheries, National Centers for Coastal Ocean Science, National Institute of Standards and Technology, and SeaWorld and Busch Gardens. We especially thank Brian Balmer, Brenda Bauer, Brian Quigley, Ross Martinson, and Larry Fulford for their valuable contributions to this research. We thank Jason Allen, Aaron Barleycorn, Sunnie Brenneman, Kerry Coughlin, James Daugomah, Sylvain De Guise, Deborah Fauquier, Gavin Goya, Larry Hansen, Craig Harms, Jean Herrman, Trip Kolkmeyer, Stephen Manley, Amanda Moors, Lydia Staggs, Jay Sweeney, Christina Toms, Blaine West, and Rob Yordi. This is the National Marine Mammal Foundation’s contribution #336 to peer-reviewed scientific literature. Data are publicly available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (doi:10.7266/N7H41PTV, 10.7266/n7-76aj-rp39, 10.7266/n7-sv57-1h12).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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