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Physiological Consequences of Environmental Contamination in an Elasmobranch with Matrotrophic Histotrophy, the Round Stingray (Urobatis Halleri)

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Physiological Consequences of Environmental Contamination in an Elasmobranch with Matrotrophic Histotrophy, the Round Stingray (Urobatis Halleri) University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2018-01-15 Physiological consequences of environmental contamination in an elasmobranch with matrotrophic histotrophy, the Round Stingray (Urobatis halleri) Lyons, Katherine Lyons, K. (2018). Physiological consequences of environmental contamination in an elasmobranch with matrotrophic histotrophy, the Round Stingray (Urobatis halleri) (Unpublished doctoral thesis). University of Calgary, Calgary, AB. http://hdl.handle.net/1880/106331 doctoral thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Physiological consequences of environmental contamination in an elasmobranch with matrotrophic histotrophy, the Round Stingray (Urobatis halleri) by Katherine Danielle Hohman Lyons A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY GRADUATE PROGRAM IN BIOLOGICAL SCIENCES CALGARY, ALBERTA JANUARY, 2018 © Katherine Danielle Hohman Lyons 2018 Abstract A range of physiological biomarkers were compared in two populations of Round Stingray (Urobatis halleri) that differed primarily in PCB exposure. Females, and their embryos, were sampled each month of pregnancy at both sites, while adult males were matched with a 40-day subset of females to investigate the effect of sex and its interaction with PCB exposure. I hypothesized that exposure would have negative energetic outcomes for PCB-exposed, compared to reference population, stingrays. Adverse impacts were widespread. Number of offspring was not affected by PCB exposure; however, exposure exacerbated maternal tissue mass, and quality, loss during pregnancy. PCB-exposed females also compromised osmoregulation with urea, an important osmolyte, reduced in maternal plasma. Higher liver quality in contaminant-exposed females was not associated with higher embryo quality, suggesting contaminants increase metabolic demands in adult females and lead to inefficiencies in embryos’ use of maternal resources. Embryos also influenced their uterine environment, as they were steroidogenic and capable of osmoregulating very early in development. I found sex- related differences in embryo mass only at the reference site, suggesting that contaminant effects on males begin in utero. These contaminant sex-related effects extended into adulthood, as relative liver mass and energy content were lower in comparably-sized adult males than females, whereas fewer differences were found between adults at the reference site. Higher energy generation potential, combined with lower tissue quality in contaminant-exposed adult males suggests they are more energetically compromised than females, despite the latter’s costly pregnancy demands. Regardless of sex, contaminant exposure had negative impacts on the ability of adult stingrays to mount a robust secondary stress response as reflected by lower plasma glucose levels after stress, thus potentially impairing their ability to respond to acute ii stressors. Effects found both in utero and in adulthood suggest that contaminants have a significant, and potentially life-long, impact on Round Stingray homeostasis. This has implications for other species with greater contaminant burdens. Contaminant exposure, and its interactive effects with sex and age, should be included as part of effective elasmobranch management. iii Acknowledgements First and foremost, I need to thank my family and friends for all of the unwavering support they provided to me while obtaining this degree. I could not have overcome all the struggles I went through without these people in my life. Specifically, and in no particular order, I want to thank my friends Ryan Freedman, Chris Bedore, Ramya Singh, Noreen Singh, Joanne Hou, Carrie Espasandin, “Arthur Cheng”, Brendan Cooper, Joe Bizzarro and my family, mom, dad and sister Rachael, who were there with me through the worst of it. I need to give a shout out to Ralph Appy who was out in the field with me every single fishing day with a smile and Dennis Noesen who generously shuttled us between the mainland and Catalina Island. Thanks to Chris Lowe for providing me lab space and storage of my samples while in the field. I need to give a mountain of gratitude to my advisor, Dr. Wynne-Edwards, for throwing me a life ring when I thought this was a sinking ship. In the much too short time Dr. Wynne- Edwards advised me, I learned so much more in four months than I did in the previous four years. Dr. Wynne-Edwards restored my faith in my science and played an incredibly instrumental role in helping me write and analyze my thesis into the strongest product it could be. I will be forever appreciative and grateful for the advice, guidance and mentorship that Dr. Wynne-Edwards has given to me. iv Dedication To the Round Stingray, whose sacrifice furthered our scientific understanding v Table of Contents Abstract .............................................................................................................................. ii Acknowledgements .......................................................................................................... iv Dedication ...........................................................................................................................v Table of Contents ............................................................................................................. vi List of Tables ......................................................................................................................x List of Figures and Illustrations ..................................................................................... xi List of Symbols, Abbreviations and Nomenclature ......................................................xv Chapter 1: Introduction ....................................................................................................1 1.1 Elasmobranch Physiology .......................................................................................1 1.2 Polychlorinated Biphenyl Contaminants ...............................................................3 1.3 Patterns of Accumulation ........................................................................................4 1.4 Organochlorine Effects in Elasmobranchs ............................................................5 1.5 Knowledge Gaps ......................................................................................................7 1.6 Round Stingray Ecology in Southern California ..................................................7 1.7 Sources of Contamination at the Mainland Site ...................................................8 1.8 Comparisons with the Offshore Site ....................................................................10 1.9 Research Objectives ...............................................................................................12 Chapter 2: Physiological Consequences of Legacy PCB Contamination in an Elasmobranch with Matrotrophic Histotrophy, the Round Stingray (Urobatis halleri): Impaired Intrauterine Development ......................................................13 2.1 Introduction ............................................................................................................13 2.2 Methods ...................................................................................................................15 2.2.1 Study sites. ......................................................................................................15 2.2.2 Sampling. ........................................................................................................17 2.2.3 Data analysis. .................................................................................................17 2.2.3.1 Environmental factors. .........................................................................17 2.2.3.2 PCB quantification. ..............................................................................17 2.2.3.3 Fecundity. ..............................................................................................19 2.2.3.4 Developmental stage. ............................................................................19 2.2.3.5 Sex-specific effects. ...............................................................................19 2.2.3.6 Embryo quality. .....................................................................................20 2.2.3.7 Intrauterine growth variability. ............................................................20 2.3 Results .....................................................................................................................20 2.3.1 Timing of ovulation. ......................................................................................20 2.3.2 Fecundity. .......................................................................................................21 2.3.3 Developmental stage. .....................................................................................21 2.3.4 Sex-specific effects. ........................................................................................24
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