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PAH Toxicity Dependence on Ingested Plant Species Dissipation and Phytotoxicity of Oil Sands Naphthenic Acids in Wetland Plants A thesis submitted to the College of Graduate Studies and Research in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Toxicology Graduate Program University of Saskatchewan Saskatoon, Saskatchewan Canada By Sarah Anne Armstrong ©Copyright Sarah Anne Armstrong, July 2008. All rights reserved. i PERMISSION TO USE In presenting this thesis in partial fulfillment of the requirements for a Doctor of Philosophy degree from the University of Saskatchewan, I agree that the Libraries of this University may make it freely available for inspection. I further agree that permission for copying of this thesis in any manner, in whole or in part, for scholarly purposes may be granted by the professors who supervised my thesis work, in their absence, by the Graduate Chair of the program or Dean of the College in which my thesis work was done. It is understood that any copying or publication or use of this thesis or parts thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of Saskatchewan in any scholarly use which may be made of any material in my thesis. Requests for permission to copy or to make other use of material in this thesis in whole or in part should be addressed to: Chair of the Toxicology Graduate Program Toxicology Centre University of Saskatchewan 44 Campus Drive Saskatoon, SK, Canada S7N 5B3 i ABSTRACT Naphthenic acids (NAs) are toxic organic acid compounds released during the caustic hot-water extraction of crude oil from oil sands in north-eastern Alberta, Canada. NAs subsequently accumulate in the large volume of oil sands process water (OSPW) produced daily by oil sands operations. The complexity of dealing with a mixture of over 200 individual NA compounds, combined with their acute aquatic toxicity and large volume of production has made them an emerging pollutant of concern for western Canada. The following thesis outlines a variety of experiments designed to determine the potential to use wetland plants to enhance the dissipation of NAs from OSPW (phytoremediation). Investigations were carried out with three native emergent macrophyte species cattail (Typha latifolia), common reed (Phragmites australis subsp. americanus), and hard-stem bulrush (Scirpus acutus) to see if they enhanced the dissipation of NAs from a hydroponic system. Dissipation of NAs (at 30 mg L-1 and 60 mg L-1) was investigated with both a commercially available NA mixture as well as with a NA mixture extracted from the OSPW. Dissipation of NAs was also investigated under the different ionized forms of NAs (ionized, pH = 7.8; and non-ionized, pH = 5.0) to better elucidate the mechanisms of NA uptake and toxicity in plants. Phytotoxicity of NAs was investigated in hydroponic experiments through fresh weight gain and evapotranspiration was monitored throughout the experiment by water uptake. Commercially available NA mixture was more phytotoxic than oil sands NAs mixture. As well, NAs were found to be more phytotoxic in their non-ionized form therefore indicating that they may be taken up through an „ion-trap‟ mechanism. However despite this, no significant dissipation of total NAs was observed from planted hydroponic systems. Nevertheless there was a significant change in the distribution (percent abundance) of individual NA families of certain size. These changes were related to the one- and two-ring NA compounds (Z = -2 and Z = -4). Despite not detecting any dissipation of total NAs from the systems, plants were able to reduce the toxicity of a NA system over 30 days by 45% as determined by Daphnia magna acute toxicity bioassays; a 11% greater reduction than unplanted systems. ii Studies were also conducted investigating the microbial community inhabiting cattail roots exposed to NAs. It was observed that the rhizosphere community changed with NA exposure, with a general increase in potentially pathogenic bacteria and a decrease in bacteria previously found to be beneficial to plant growth. The observed microbial community change could be an indirect effect of the phytotoxicity experienced by aquatic macrophytes exposed to NAs. Synchrotron-sourced, fourier transform microspectroscopy analysis of root cross sections revealed that there were significant physiological changes to those roots exposed to NAs. These changes were identified as being cell death in the plant root epidermis as well as a change in the chemistry of parenchyma cells in the root pith. It is not known if these changes are a direct effect of NAs to the plant or due to changes of the associated rhizosphere community in the roots or some combination of both these factors. iii ACKNOWLEDGEMENTS I would like to thank my supervisors Dr. John Headley and Dr. Jim Germida for their guidance throughout this project as well as providing me with many opportunities throughout my graduate studies. I also would like to thank the other members of my advisory committee, Dr. Dena McMartin, Dr. Monique Dubé, Dr. Hans Peterson and Dr. Barry Blakley for assisting throughout the completion of this thesis and for providing various aspects of scientific expertise. My gratitude also goes out to Dr. Jan Ciborowski from the University of Windsor for being the external examiner for this thesis. Additionally I would like to thank the following people for providing technical assistance who were integral to the completion of this project: Kerry Peru, Lori Phillips, Dr. Susan Kaminskyj, Dr. Luca Quaroni, Dr. Jay Dynes, Dr. Michael Pollock, Dr. Colleen Christensen, and Arlette Seib. This thesis is dedicated to the memory of Karen Cooper-Calhoun (1979-2007) my friend, who without her, I would not have survived my first years of undergrad and made it into graduate studies in the first place. To my immediate family (Mom Dad and Bruce) and extended family for cheering me on and keeping my spirits up when times were tough. To my friends old and new especially Carrie Rickwood, Allison Squires, Sandra Kuchta, Julie Roy, Chris Roy, Wai Ma, Erin Thompson, Jessika L‟Heureux, Monique Wismer, Lindsay Tallon, Kristen Steele, Fiona Mackenzie, and Amy Sangster for being a constant support through grad school. Finally I would like to thank my colleagues in the Department of Soil Science and Toxicology Centre at the University of Saskatchewan, and the National Hydrology Research Center for their support and friendship. Thank you for making the past three years such a memorable experience. Funding for this project was provided by the National Science and Engineering Research Council (NSERC) and the Program of Energy Resource Development (PERD). iv TABLE OF CONTENTS PERMISSION TO USE ....................................................................................................... I ABSTRACT ........................................................................................................................ II ACKNOWLEDGEMENTS .............................................................................................. IV TABLE OF CONTENTS ................................................................................................... V LIST OF TABLES ............................................................................................................. X LIST OF FIGURES ......................................................................................................... XII LIST OF ABBREVIATIONS ...................................................................................... XVIII 1.0 GENERAL INTRODUCTION.................................................................................... 1 1.1 PHYSICAL AND CHEMICAL PROPERTIES OF NAPHTHENIC ACIDS .......................... 5 1.2 FATE OF NAPHTHENIC ACIDS IN THE ENVIRONMENT ........................................... 6 1.3 TOXICITY OF NAPHTHENIC ACIDS ........................................................................ 8 1.3.1 Fish .............................................................................................................. 8 1.3.2 Aquatic invertebrates .................................................................................. 9 1.3.3 Mammals................................................................................................... 10 1.3.4 Plants and algae......................................................................................... 10 1.4 ANALYTICAL METHODOLOGIES FOR NAPHTHENIC ACIDS ................................. 15 1.4.1 Negative ion electrospray mass spectrometry ........................................... 15 1.4.2 Extraction and analysis in tissue matrices ................................................ 16 1.5 PLANT UPTAKE OF ORGANIC CHEMICALS .......................................................... 17 1.5.1 Uptake of naphthenic acids by plants ....................................................... 18 1.6 PLANT BIOTRANSFORMATION OF XENOBIOTICS ................................................ 19 1.7 CONSTRUCTED WETLANDS FOR CONTAMINATED WATER TREATMENT ............. 20 1.7.1 Oil sands process water and plant growth ................................................. 21 1.7.2 Emergent macrophytes.............................................................................. 22 1.8 MICROBIAL DEGRADATION OF NAPHTHENIC ACIDS .......................................... 24 1.9 USE OF FRESHWATER MACROPHYTES FOR PHYTOTOXICITY TESTING ............... 27 1.10 RESEARCH OBJECTIVES ....................................................................................
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