Date of Award

2020

Degree Type

Dissertation

Degree Name

Doctor of Philosophy in Oceanography

Specialization

Chemical Oceanography

Department

Oceanography

First Advisor

Rainer Lohmann

Abstract

Despite their ubiquity in the environment, large data gaps exist surrounding the distribution, biotic accumulation, and possible impacts of many high priority organic pollutants, particularly those considered emerging contaminants. Emerging pollutants, or contaminants of emerging concern (CECs), represent a dynamic and rapidly evolving group of substances, some of which have been extant for decades. Chapter 1 provides background about CECs covered in this dissertation, and highlights key data gaps explored within this work.

The first three manuscripts of this dissertation (Chapters 2 – 5) focus on per- and polyfluoroalkyl substances, or PFAS. PFAS are a family of CECs that demonstrate amphiphilic or hydrophilic environmental behaviors, and thus are ubiquitously distributed in aqueous and biological matrices. PFAS are associated with adverse effects in humans and wildlife at very low concentrations, and thus their biological behavior and impacts are under a great deal of scrutiny. Little work over the past two decades has evaluated these chemicals in marine food webs along the US East Coast, despite the proximity of this region to major human population centers and PFAS point sources. Tandem mass spectrometry and high-resolution mass spectrometry techniques were applied to tissue samples collected as part of a large-scale necropsy program to derive PFAS measurements in seabirds from the US East Coast. Names, Chemical Abstracts Service (CAS) number, and potential sources of each PFAS measured in this work are provided in Appendix B.

Chapter Two measured PFAS in seabird juveniles from three habitats along the US East Coast representing a range of exposure potential. Seabirds collected downstream from a major fluoropolymer production site contained the highest concentrations of legacy and novel PFAS, surpassing toxicity reference values established in controlled studies for avifauna. The novel PFAS Nafion by-product 2 (Nafion BP2) was detected in seabirds from all habitats, marking the first identification of this compound in biota beyond the industrially influenced Cape Fear region in North Carolina. Perfluorooctanesulfonic acid (PFOS) and perfluorononanoic acid (PFNA) were associated with decreased phospholipid levels, marking the first time this trend has been observed in a wild population. Chapter Three examined novel and legacy PFAS in Great Shearwaters from Massachusetts Bay over 2010 – 2019. PFOS and perfluorooctanesulfonamide (FOSA) decreased over the time series, while perfluoroalkyl carboxylic acids (PFCAs) and the novel PFAS 7:3 fluorotelomer carboxylic acid (7:3 FTCA) showed no clear trends over time. Multiple PFAS were significantly associated with morphometric variables, with increased PFAS levels associated with reduced organ weights and reduced fat depth in Great Shearwaters. Perfluorohexanesulfonic acid (PFHxS) and PFNA were negatively associated with mass of ingested plastic, marking the first time any relationship has been identified between plastic consumption and PFAS levels in a seabird. This relationship likely reflects the amphiphilic nature of PFAS that reduces the likelihood of sorption to plastic items in aqueous matrices, as well as the divergent exposure pathways for these two pollutant groups, as seabirds are primarily exposed to PFAS via diet as opposed to direct ingestion of plastics via discovery in the environment. Chapter Four assessed PFAS in eight tissues obtained from juvenile seabirds collected from three habitats along the US East Coast, the same habitats assessed in Chapter Two. These tissue-specific measurements suggested blood, liver, kidney, and lungs are primary reservoirs of PFAS in seabirds. Novel per- and polyfluoroalkyl ether acids (PFEAs) preferred blood compared to liver, suggesting reduced compatibility with the binding environment of liver fatty acid binding protein that drives PFAS uptake in liver. These results were also the first to measure novel PFEAs in brain tissue, indicating these compounds are capable of surpassing the highly selective blood-brain barrier in vertebrate wildlife.

Chapter Five focuses on microplastics, another type of CEC. Microplastics are a pervasive pollutant in aquatic ecosystems and ingestion of plastics is associated with an increased risk or mortality in seabirds. Chapter Five examined plastic ingestion in 175 Great Shearwaters from 2010 – 2019, collected at multiple locations relevant to their annual cycle across the North and South Atlantic Oceans. Each bird contained an average of 8 plastic fragments, and more than 50% of individuals contained greater than 0.1g plastic, significantly surpassing the ecological threshold suggesting no more than 10% of a given population should contain greater than 0.1g ingested plastic. Breeding adults from the South Atlantic ingested plastic less frequently (~60%), while 98% of juveniles from Massachusetts Bay were found to contain ingested plastics. Each plastic fragment was assessed using Fourier-transform ion spectroscopy to discern polymer identity. We found low- and high-density polyethylene fragments dominated within all years and locations. Breeding adults contained a higher proportion of larger polypropylene fragments compared to juveniles and non-breeding adults; breeding adults in Massachusetts Bay likewise ingested marginally larger plastic items compared to Massachusetts Bay juveniles but this was outside the limits of significance defined within the study. The abundance of larger plastic items in breeding and non-breeding adults is likely indicative of an increased use of remote, pelagic habitats subject to reduced inputs of smaller, land-derived plastics due to size-mediated distribution in the pelagic environment. Different signatures of polymer type and size between breeding and non-breeding mature birds likewise suggests rapid turnover of ingested plastics commensurate with migratory stage and location.

Chapter Six of this study leverages the vast amount of necropsy data derived in support of the included contaminant studies to correct the record regarding plumage and age characteristics of Great Shearwaters. Necropsy efforts demonstrated Massachusetts Bay is dominated by juvenile Great Shearwaters, with juveniles making up over 90% of collected birds considering the entire necropsy sample set. Nape plumage has been previously associated with individual age, with the suggestion that mature individuals possessed a completely white nape while the nape area of younger individuals was interrupted by variable amounts of brown or gray. Necropsy data collected herein suggest nape plumage is not a reliable indicator of age. Instead this data suggests nape plumage may be associated with sexual behaviors, as completely white napes were more abundant in females of all ages.

These results highlight the utility of necropsy efforts to explore multiple complimentary scientific questions within a given species, and raise further questions about Great Shearwater demographics, PFAS, and plastic ingestion. The abundance of juvenile birds in the bycatch sample set and overall Massachusetts Bay region raises questions about the impact of commercial fishing activities on Great Shearwater population, as fishing activities remove hundreds to thousands of pre-reproductive individuals from the population each year. This work also demonstrates the ability of several novel PFAS to bioaccumulate in seabirds, and indicates the need for significantly more research describing the bioaccumulation potential of new PFAS formulations in a wider range of wildlife. Additionally, these data suggest potential impacts of PFAS at environmentally relevant, ongoing exposure levels, with uncertain population-scale impacts of reduced organ weights, altered fat storage or expression, and morphological alterations. Further research should evaluate the effects of legacy and novel PFAS in marine biota with a focus on potential implications for individual and population health considering the importance of body condition and lipid stores on bird migratory and reproductive ability. Plastic ingestion in Great Shearwaters likewise merits additional investigation; over 50% of individuals evaluated in the study contained more than 0.1g of ingested plastic, surpassing a threshold established as problematic for seabird plastic ingestion. Further work should evaluate trends of plastic ingestion over time using harmonized methods to leverage the Great Shearwater as a sentinel for specific Atlantic habitats and monitor for potential impacts.

Within a management context, these results provide justification for continued investigation and potential phase-out or regulation of novel PFAS akin to some legacy formulations, considering their potential for long-range transport and bioaccumulation within offshore ocean biota demonstrated within this work. Additionally, the demonstrated abundance of long-chain PFCAs in seabirds demonstrates the importance of considering the downstream environmental transformations and impacts of PFAS currently in use. Long-chain PFCAs are rarely manufactured purposefully, but may form as production by-products from creation of other PFCAs or may form in the environment or in biota via oxidation of precursor compounds. The abundant downstream bioaccumulation of these inadvertently created compounds suggests the total environmental life-cycle of a given PFAS should be evaluated to prevent formation of bioaccumulative and ubiquitous terminal end products like long-chain PFCAs or 7:3 FTCA. This work additionally underscores the importance of policies and practices that support waste management and effective recycling, considering upwards of 90% of plastic items found within seabirds were recyclable polymers that likely ended up in the environment due to waste mismanagement.

Available for download on Sunday, December 19, 2021

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