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(Catostomus Commersoni) EXPOSED to OIL SANDS Journal of Toxicology and Environmental Health, Part A, 69:967–994, 2006 Copyright© Taylor & Francis Group, LLC ISSN: 1528–7394 print / 1087–2620 online DOI: 10.1080/15287390500362154 CYP1A INDUCTION AND BLUE SAC DISEASE IN EARLY LIFE STAGES OF WHITE SUCKERS (Catostomus commersoni) EXPOSED TO OIL SANDS Maria V. Colavecchia1,2, Peter V. Hodson2, Joanne L. Parrott1 1Environment Canada, Science and Technology Branch, Burlington, Ontario, Canada 2Queen’s University, School of Environmental Studies, Kingston, Ontario, Canada The objectives of this study were to evaluate the influence of natural oil sands on the early developmental stages of white sucker (Catostomus commersoni) and to determine whether biochemical responses in this species were similar to native fish caught in the Athabasca Oil Sands area. Early life stage (ELS) sediment toxicity tests were conducted using controls, refer- ence sediments, natural oil sands, and industrially contaminated (wastewater pond) sediments collected from sites along the Athabasca River, Alberta (Canada). Eggs and larvae were observed for mortality, hatching, deformities, growth, and cytochrome P-4501A (CYP1A) activ- ity using immunohistochemistry. E-Nat-, S-Nat-, and wastewater pond sediment-exposed groups showed significant premature hatching, reduced growth, and exposure-dependent increases in ELS mortality and larval malformations relative to controls. The most common lar- val deformities included edemas (pericardial, yolk sac, and subepidermal), hemorrhages, and spinal defects. Juveniles exposed to oil sands and wastewater pond sediments (96 h) demon- strated significantly increased 7-ethoxyresorufin–O-deethylase (EROD) activity (30- to 50-fold) as compared to controls. Reference sediment-exposed groups and water controls demon- strated reliable embryo and larval survival, minimal malformations, and negligible CYP1A stain- ing. These observed signs of blue sac disease (ELS mortality, malformations, growth reductions, CYP1A activity induction) may produce deleterious reproductive effects in natural fish popula- tions exposed to oil sands mixtures. Received 21 March 2005; accepted 26 May 2005. This research was funded by grants from the Toxic Substances Research Initiative (Project 187) through Health Canada, Panel on Energy Research and Development, and the Natural Sciences and Engineering Council of Canada (PVH). M. Colavecchia was supported by scholarships awarded by OGS, Canadian Net- work of Toxicology Centres, and Petro-Canada. The authors thank the following individuals for their techni- cal assistance with the field sampling program: R. Neurtherander (NWRI), B. Crosley, M.Conly (CWS), Golder Associates (K. Allen and M. Ezekiel), Regional Aquatics Monitoring Program, Suncor Energy (A. Cum- mins), Syncrude Canada (T. VanMeer, N. Rutley), M. Bowerman, and A. Winchester (Queen’s University). We thank G. Fodor (DFO), Dr. P. Akhtar (Queen’s University), B. Blunt, M. Baker (NWRI), S. Cagampan, and S. Backus (NLET) for their enthusiastic laboratory assistance. Portions of this research were presented at the 2003 Annual Aquatic Toxicity Workshop (Thirtieth Annual Meeting Abstracts, p. 90). Useful comments by Dr. S. Kacew and two anonymous reviewers helped improve an earlier draft of this article. Address correspondence to Maria V. Colavecchia, Environment Canada, Science and Technology Branch, Burlington, Ontario, L7R 4A6, Canada. E-mail: [email protected] 967 968 M. V. COLAVECCHIA ET AL. INTRODUCTION Oil sands mining is a large and growing industry in the Athabasca region of northern Alberta, Canada. The Athabasca Oil Sands is the largest of 4 oil depos- its in the province with an estimated 1.7 trillion barrels of bitumen (Alberta Department of Energy, 1995). Bitumen is a naturally weathered, heavy crude oil composed of a complex mixture of hydrocarbons, heteroorganics, and metals. Headley et al. (2001) recently characterized the degree of natural polyaromatic hydrocarbons (PAHs) in this region and showed that tributary sediments contain significant levels of PAHs, particularly alkyl-substituted PAHs (0.01 to 34.7 μg/g). Surface waters in the Athabasca River basin contain PAHs and naphthenic acids (NAs) derived naturally from the erosion of bitumen deposits along the banks of rivers and from riverbeds. The main chemical compounds in semipermeable membrane device (SPMD) dialysates from surface waters in this region are PAHs, alkyl-PAHs, NAs, benzothiophenes, and methyl carbazoles (Parrott et al., 1996). Increased 7-ethoxyresorufin O-deethylase (EROD) activity in cultured fish cells exposed to these extracts indicates that fish are exposed to naturally occurring oil sands related compounds (OSRCs) that are capable of inducing mixed-function oxygenase enzyme (MFO) activity (Parrott et al., 1996). There are also OSRCs originating from oil sands extraction activities. Syn- crude Canada Ltd. and Suncor Energy, recover oil adjacent to the Athabasca River, producing large volumes of wastewaters (tailings). Researchers have assessed several endpoints in native yellow perch (Perca flavescens) stocked in tailings ponds, and found elevated EROD activity and bile PAHs metabolites (van den Heuvel et al., 1999). In addition, exposed perch exhibited increased gill pathologies and skin lesions that were correlated with the concentrations of OSRCs (van den Heuvel et al., 2000). As industries expand production and open new mines, concerns related to the potential detrimental impacts on aquatic ecosystems are growing. There is a need to determine the possible effects arising from OSRCs leaching from sediments, from both anthropogenic and natural source areas. While the toxicity of tailings waters was documented, few data exist on the effects of natural oil sands on indigenous species. Recent studies showed altered biochemical and reproductive responses in native fish species residing in the Athabasca oil sands relative to reference fish (Tetreault et al., 2003a). Native slimy sculpin (Cottus cognatus) and pearl dace (Semotilus margarita) residing within nat- ural oil sands showed reductions in steroid production and increased EROD activity relative to reference areas. Wild adult longnose suckers (Catostomus catostomus) captured in oil sands areas demonstrated a 15-fold increase in EROD activity as compared to reference fish (Parrott et al., 1999). Although researchers did not find effects on body condition, these studies provided valuable baseline information important for future environmental monitoring in this region. Early life stages (ELS) of fish exposed to weathered crude oils (Couillard, 2002; Carls et al., 1999; Marty et al., 1997a, 1997b), oil sand extracts (Rhodes et al., 2005), and natural oil sands (Colavecchia et al., 2004) demonstrated BLUE SAC DISEASE IN WHITE SUCKERS EXPOSED TO OIL SANDS 969 significant toxicological responses that have been linked to PAHs exposure. Fathead minnows (Pimephales promelas) exposed to natural oil sands and waste- water sediments showed exposure-related increases in ELS mortality, larval mal- formations, and reduced size. Differential toxicity among sites was related to sediment PAHs concentration and composition, specifically alkyl-substituted PAHs (Colavecchia et al., 2004). In general, sediment PAHs in natural oil sands (250–360 μg/g TPAH) were predominantly composed of alkylated derivatives of phenanthrene/anthracene, fluoranthene/pyrene, and benz[a]anthracene/ chrysene. High concentrations of alkylated benz[a]anthracene/chrysene and benzofluoranthene/pyrene compounds were detected in the refinery waste- water pond sediments (1300 μg/g TPAH). Since little is known about the toxicity of alkylated PAHs to the ELS of teleosts (NRC, 1985), it is important to assess whether PAHs and other OSRCs are bioavailable and have the potential to pro- duce effects in fish. The objectives of this study were to assess the effects of OSRCs (both natu- rally occurring and those due to anthropogenic inputs) on the ELS of white suckers (Catostomus commersoni). The wide natural distributions of this spe- cies make it an ecologically relevant species for many areas of North America (Nelson & Paetz, 1992). Preliminary assessments of native adult suckers in the Athabasca Oil Sands region indicate this species was exposed to naturally occurring OSRCs, with reduced gonad size as compared to upstream fish (Par- rott et al., 1999). Impacts on ELS were assessed in terms of hatching success, time to hatch, larval development, growth, and survival. Several studies dem- onstrated EROD induction in fish following lab exposure to PAHs and crude oils (van der Weiden, 1994; Marty et al., 1997b). A second objective was to evaluate whether a laboratory exposure of juvenile fish to oil sands sediments could produce biochemical responses (EROD induction) similar to those of fish caught in the Athabasca Oil Sands area. MATERIALS AND METHODS Sediment Collection In October 2001, surface sediments were collected from two tributaries of the Athabasca River, namely, the Ells River and the Steepbank River, Alberta, Canada (Figure 1). In each of these tributaries, river sediments were collected from downstream (natural) and upstream (reference) sites. The downstream sam- ples were collected within the oil sands deposit where there are natural PAHs inputs (E-Nat, 57°16.01′N/111°42.51′W, and S-Nat, 57°1′23”N/111°28′30”W), whereas the reference sediments were taken upstream, outside of the oil sands deposits (E-Ref, 57°13.52′N/111°53.15′W, and S-Ref, 56°55′40”N/ 111°13′56”W). In addition, sediments
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