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Estrogens, Endocrine Disruption, and Approaches to Assessing Gametogenesis and Reproductive Condition in Freshwater Mussels (Bivalvia: Unionidae)

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Estrogens, Endocrine Disruption, and Approaches to Assessing Gametogenesis and Reproductive Condition in Freshwater Mussels (Bivalvia: Unionidae) Estrogens, Endocrine Disruption, and Approaches to Assessing Gametogenesis and Reproductive Condition in Freshwater Mussels (Bivalvia: Unionidae) Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy In the Graduate School of The Ohio State University By David M. Sovic, B.S. Graduate Program in Environmental Science The Ohio State University 2016 Dissertation Committee: Roman P. Lanno, Advisor G. Thomas Watters Susan Fisher Linda Weavers Copyright by David M. Sovic 2016 Abstract Organisms belonging to the family Unionidae, commonly referred to as freshwater mussels, unionids, or pearly mussels, have, over the last several decades, experienced drastic declines in range and number. These declines have not been localized to a particular region and have not been specific to any particular environment or habitat, but have been experienced by a great number of the species belonging to this diverse group. While a variety of potentially causative factors have been implicated in the decline of Unionids worldwide, the possibility that environmental contaminants, including those identified or suspected as endocrine disrupting chemicals (EDCs), might contribute to observed unionid declines is central to this work. Unionid bivalves are long-lived, sessile creatures that, by actively filter feeding, are at risk of a high degree of exposure to water-borne xenobiotics. Ecotoxicological research on potential endocrine disruptive effects on bivalves, and in particular many unionids, however, presents a unique challenge due to the highly endangered, and thus protected, nature of many of these species and a, generally, limited ability to secure and maintain organisms for testing. The ability to assess effects of toxicant exposure in both laboratory and field studies on unionid reproductive condition and gametogenic development using minimally invasive and nonlethal methods is paramount to the ability to gain information for such species. Typical methods used to assess reproductive development and gametogenesis in bivalves focus on histological analyses, which have most always required organism sacrifice. Recent advances in nonlethal assessment and methodological developments focused on the utilization of nonlethal procedures has, however, provided a new avenue by which evaluation of potential exposure effects might be evaluated. Therefore, this ii study aimed first to test the ability of a nonlethal gonad biopsy to provide information sufficient for accurate gametogenic assessment of the common unionid, Elliptio complanata. E. complanata utilized in this study were collected at one of two sites in the Cacapon River of West Virginia (WV). Spring and summer sampling was conducted in order to assess the ability of the biopsy procedure to stage gametogenesis at different points of the reproductive cycle. A biopsy of gonadal fluid was collected from each organism, and the individuals were then sacrificed and preserved for histological analysis in order to make possible a known method of gametogenic staging for comparison and validation of biopsy-based stage determinations. Data obtained using both the histological and biopsy-based approach were compared, and method of biopsy analysis was generated that resulted in a high degree of agreement between histological and biopsy stage determinations. Limitations of the procedure were noted, including a lack of fully representative samples of the various gametogenic cell stages in the biopsy. The influence of this limitation appeared to be more influential to female analysis, however the biopsy procedure was found to predict histological stage determinations with a high degree of accuracy for both sexes of E. complanata, at various stages of development. This procedure was further validated using a similar species, Elliptio insulsa as part of a study on the effects of 17β-estradiol (E2) exposure on gametogenesis and reproductive development in this species. As a high prevalence of intersex condition has been observed for fish populations residing in the Cacapon River and surrounding river systems, similar effects on reproduction and gamete development were studied for E. complanata in the Cacapon River. The field research sites identified in this study were located in the most upper (Site 1) and lower (Site 2) reaches of the Cacapon, and were associated with land use activities characterized by mainly agricultural activity (Site 1) or forest (Site 2). Of primary ecotoxicological interest to Site 1 land use is the high iii concentration of poultry farming that occurs in this region, and the associated land-application of litter waste that has been shown to potentially contain elevated levels of the primary vertebrate estrogen, E2 and its primary metabolite, estrone (E1), among other potentially toxic xenobiotics. Rates and timing of application of these wastes, and potential over-application associated with an overabundance of litter in the region, may influence the risk of area surface waters receiving runoff contaminated with these estrogenic compounds and, in turn, might increase the risk of exposure to resident mussels. Whether vertebrate estrogens play an active role in any reproductive or physiological processes in unionids is currently debated. While a growing body of evidence appears to suggest effects in these organisms following exposure to a variety of estrogenic compounds, including known EDCs, often these exposures are to complex mixtures in the environment, such as sewage treatment plant (STP) effluents that demonstrate some degree of estrogenic activity, while other studies have been criticized for experimental design flaws, a lack of replication, or an absence of quantitative response measures. Apparent impacts on gamete development were observed, particularly for male E. complanata at Site 1, as a high degree of variance in gamete production was observed for samples collected from this population, particularly in comparison to samples collected from Site 2. In addition, a relocation study on organism growth and gamete development suggests that Site 1 organisms are experiencing growth inhibition and, possibly, increased rates of gamete resorption, though this latter observation could not be statistically verified. In conjunction with organism sampling at each site, passive sampling devices, known as Polar Organic Chemical Integrative Samplers (POCIS) were deployed during different periods of the year at each site, and extracts were evaluated for their total estrogenic activity using the iv recombinant yeast estrogen screen, or YES assay. Results of these tests suggest that the estrogenic character of Cacapon River surface waters is variable, but support the general presence of some chemical(s) that contain inherent estrogenic activity. In order to further test whether vertebrate estrogens effect unionid gamete development, E. insulsa were exposed in the laboratory to varying doses of E2. Organisms were initially sexed and individuals of each gender were randomly placed into one of four exposure groups. Groups were defined by exposure level; “High Dose” (19 ng/µL E2), “Intermediate Dose” (1.9 x 10-2 ng/µL E2), “Low Dose” (1.9 x 10-5 ng/µL E2), or solvent control and were injected with E2 at the start of the experiment, and, again, after five days. A biopsy of gonad was then collected 10-days after the initial dosing event, and again five months after the start of the experiment, after a period of expected active gametogenic development. Organisms were also sacrificed at that time for histological analysis. No significant effects on gamete development were observed for female E. insulsa in any exposure group, however, after the five month period, male E. insulsa were found to exhibit a significant decrease in gamete production in all exposure groups, relative to controls. These effects were observed in histological samples, however similar effects were not detected in analysis of biopsy tissues, though the depressed gamete development among these males is similar to findings for male E. complanata located at Site 1 during field studies, as the same metric was analyzed and a high degree of variance was detected within this sample of the Site 1 population. The application of this biopsy method of gametogenic assessment was also utilized for the federally endangered unionid species, Pleurobema clava. Previous surveys had found that one P. clava population, located in the East Fork West Branch St. Joseph River in Michigan (MI) was exhibiting a lack of recruitment and apparent cessation of reproduction. The population was v characterized by old, large individuals and no young organisms. Therefore, an investigation was undertaken with the objective to identify the stage, or stages, at which reproduction was failing in this population, in order to better guide future conservation efforts. Additionally, POCIS samplers were deployed seasonally in order to determine the presence or absence of estrogenic compounds in the surface waters proximate to these organisms. An additional study site for P. clava was located in the Allegheny River near Tionesta, Pennsylvania (PA) and served as a reference site for this study, and a surrogate species, Elliptio dilatata was sampled concurrently as sample sizes of P. clava were limited due to the highly endangered status of this species. Sampling of P. clava in the East Fork indicates recent successful recruitment in this population, as a number of very young organisms were collected and positively identified. However,
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