Contamination Through Deforestation and Oil Extraction in the Andean

Environmental Contamination of Fish and Humans through Deforestation and Oil Extraction in Andean Amazonia

Jennifer Webb

Department of Geography McGill University, Montreal

June 2010

A thesis submitted to McGill University in partial fulfilment of the requirements of the degree of Doctor of Philosophy

1 Abstract This dissertation assesses the levels of mercury in fish and human populations and PAHs in local communities along three rivers in the Ecuadorian and Peruvian Amazon. Land use changes in the Amazon are begetting numerous negative impacts on both ecosystems and local populations. One negative consequence of deforestation is the contamination of local ecosystems by mercury (Hg), a potent neurotoxic agent, which is leached from soils when river-side plots are cleared. In the Andean Amazon, the incursion of petroleum companies has led to road construction, colonization and areas of intense deforestation. The techniques used in the extraction of oil in this remote and overlooked region have left a legacy of contamination, specifically heavy metals such as Hg and polycyclic aromatic hydrocarbons (PAHs). Limited research has evaluated the degree of Hg contamination in the Andean Amazon and less research still has determined the state of contamination as a result of oil extraction. The purpose of this research is to uncover the extent of contamination in fisheries and human populations reliant on the fish and water resources of the area.

Eight communities along three white water rivers – the Napo River (Ecuador), the Corrientes River (Peru) and the Pastaza River (Peru) – with differing degrees of deforestation and oil extraction were studied. Questionnaires were administered to 192 people who accepted to provide hair samples. Samples of commonly eaten fish were collected. A subsample of the study population (n=76) also provided a urine sample. Biological samples of fish (n=486), human hair and urine were analysed for Hg and samples of urine were analysed for 1-hydroxypyrene (1- OHP), a metabolite of one of the most common PAHs. Regression analysis was used to draw links between contamination levels and socio-demographic, dietary and occupational characteristics of the population. One health outcome – miscarriages – was evaluated in the questionnaires and examined in light of contamination levels.

i Hg levels in some predatory fish species exceed World Health Organization (WHO) recommendations (range = 0.001-2.97 μg/g). Fish from a heavily contaminated micro watershed were found to have bioaccumulated more Hg. Hair-Hg levels in humans (range = 1.07-24.78 μg/g) were found to be significantly related to number of fish meals consumed per week. Hg levels in urine (range = 0.02-15.62 μg/g creatinine) were dependant on source of washing water for women and work cleaning up an oil spill for men. Concentrations of urinary 1-OHP (range = 0.03-1.62 μmol/mol creatinine) were likewise related to source of washing water in women; but, in men, the most significant variable was bottom-dwelling fish species as most commonly eaten fish. The one health outcome examined in this dissertation showed that the number of miscarriages a woman reported was significantly associated with higher levels of 1-OHP. Results were communicated to the community members through a theatrical play. The play was intended to provide information that would help people reduce their exposure to contaminants while maximizing nutritional intake from fish. The play was narrated by the research team and community members were incorporated as actors.

The primary conclusions drawn from these findings are that petroleum extraction is leading to increased levels of Hg in fish and humans and increased concentrations of PAHs in local people. At least one negative health outcome of exposure to PAHs – miscarriages – has been shown to be associated with higher levels of contaminants in the bodies of women. Theatre was found to be a successful method for engaging participants, eliciting comments and questions and fostering a genuine interaction with the community.

ii Résumé Cette thèse examine et compare les niveaux de mercure et de HAP dans les communautés riveraines de trois bassins de l’Amazonie péruvienne et équatorienne. Les impacts des changements de vocation des terres en Amazonie sont multiples, tant sur les écosystèmes que sur les populations qui en dépendent. Une des conséquences du déboisement est la contamination des écosystèmes aquatiques par le mercure (Hg), un puissant neurotoxique, dû à l’érosion des berges et la migration de ce métal lourd contenu dans les sols. En Amazonie andine, l’incursion des compagnies pétrolières a mené à la construction de route, la colonisation et la déforestation de vastes pans de forêt. Les méthodes d’extraction pétrolière utilisées dans ces régions isolées et souvent ignorées ont entraîné un legs de pollution en métaux lourds (dont le Hg) et en hydrocarbures aromatiques polycycliques (HAP). Peu d’étude ont évalué l’amplitude de la contamination au Hg en Amazonie andine et encore moins ont évalué celle liée à l’extraction pétrolière. Le but de cette recherche est de déterminer le spectre de ces contaminations dans les poissons et les communautés riveraines amazoniennes dont la diète en dépend.

Cette étude porte sur 8 communautés basées dans 3 bassins de rivière à eaux blanches (Napo (Équateur), Corrientes (Pérou) et Pastaza (Pérou)) au niveau de déboisement et d’extraction pétrolière distincts. 192 personnes ont participé à l’étude et à la collecte d’échantillon de cheveux. Un sous-groupe (n = 76) de cette population à l’étude a participé à la collecte d’échantillon d’urine. Des échantillons des poissons les plus fréquemment consommés furent prélevés (n=486). Les niveaux de Hg et de 1-hydroxypyrene (1-OHP), un métabolite d’un des HAP les plus communs, furent mesurés dans les échantillons de cheveux, d’urine et de poisson. Des régressions linéaires furent utilisées pour identifier les corrélations entre les niveaux de contamination et les caractéristiques sociodémographiques, diététiques et occupationnelles des populations à l’étude.

iii Les niveaux de Hg dans certains poissons prédateurs excèdent ceux recommandés par l’Organisation mondiale de la santé (entre 0.001-2.97 μg/g) et on observe chez les poissons provenant de micro bassins versants fortement contaminés une plus forte bioaccumulation en Hg. Les résultats montrent une corrélation significative entre les niveaux de Hg dans les cheveux (entre 1.07-24.78 μg/g ) et le nombre de repas hebdomadaires contenant du poisson. Les niveaux de Hg dans l’urine (entre 0.02-15.62 μg/g créatinine) montrent une dépendance envers les sources d’eaux utilisées pour le lavage par les femmes et les travaux de nettoyage de déversement pétrolier chez les hommes. Les concentrations en 1-OHP dans l’urine (entre 0.03- 1.62 μmol/mol créatinine) sont aussi reliées aux sources d’eaux employées par les femmes tandis que chez les hommes, la corrélation observée pour ce contaminant est liée à la consommation de poisson de fond comme espèce préféré. Les femmes avec des niveaux plus élevés de 1-OHP dans l’urine montrent de plus hauts taux de fausse-couche. Les résultats de cette étude furent présentés par l’équipe de recherche aux communautés sous forme de théâtre participatif visant à fournir l’information nécessaire pour diminuer les risques d’exposition au contaminant tout en maintenant une diète équilibrée.

La somme des résultats mène à conclure que l’activité pétrolière entraîne une augmentation des niveaux de Hg dans les poissons et les populations qui les consomment tout en entraînant une augmentation des niveaux de HAP dans ces mêmes populations. La divulgation des résultats sous forme de pièce de théâtre semble une méthode adéquate pour engager la population, entraîner une réflexion et encourager une interaction dynamique entre l’équipe de recherche et les communautés.

iv Acknowledgements In the preparation of the material in this dissertation, I would like to thank first of all my supervisor, Oliver Coomes, who never failed to get me my chapters back before I could have ever imagined possible. I’d like to thank him for all the advice and constructive comments he provided. I would also like to thank him for being there for me during all of the events that marked the last five years. Your support and words of wisdom were invaluable to me. My committee members, Nancy Ross and Donna Mergler, provided guidance and support throughout my research. They are both a real inspiration to me. I would also like to thank Isabelle Rheault of the GEOTOP, UQAM laboratory and Robert Lemieux of the First Nations and Inuit Health Branch Laboratory (FNIHBL), Health Canada in Ottawa for all their help with the lab analyses. Sébastian Breau of the Department of Geography, McGill University, and Charles DeBlois of UQAM helped with some of the statistical analysis. Sylvain Archambault provided his exceptional mapping skills and amenable demeanor in pulling together the map to the study area with very few resources.

This research was only possible as a result of the support that we had from our Ecuadorian and Peruvian collaborators. As usual, Edy Quizhpe went over and beyond what was expected of him as a collaborator on this project. You rock Edy! A very special thanks to Mauricio Delfin, who accompanied us on our last trip to perform the play and make a video. What a team we made! Oscar Betancourt, Fredy Yumbo, Domingo Grefa and Myriam and Oscar in Ecuador and Ruth Arroyo, Carlos Rengifo, Cesar Gil Perleche, Josué Yacum Tello, José Yacum and Aurelio Chino in Peru were invaluable aids in carrying out the methodology as well as great friends. Betsy Valderramo y Miraluz Cueva made the costumes used in the play. Each community welcomed us and helped us in its own way. Three families in particular stood out above all others: the Mamallacta-Yumbos from Añangu, the Grefas from Palma Roja and the Chinos from Loboyacu. I would like to warmly thank all members of these families for their hospitality. Other community members were also actively involved in the realization of this study.

v Thanks to Issac Mucushua Cariagano, Dionisio Mucushua Sandi, River Mucushua Sandi, Miriam Roncald Guerreo, Jiovanny Rivendera, and David Grefa. We received help, feedback and interest from several local organizations and their members. Thanks to the people at Shinai: Carol Burga, Lorenzo Grimaldi, Wendy Pineda, Martin Vasquez; the World Wildlife Foundation: Hernán Flores Martinez, Geanina Lucana Peralta; FEDIQUEP: Aurelio Chino, Wilson Maca Chino; and FECONACO: Henderson Rengifo. Others who work on the protection of the Andean Amazon have been an inspiration: Christopher Canaday, Miguel San Sabastian, Jorge Rivadeneyra, Judy Logback, Erika Andersson, and Nixon Revelo. Researchers outside of the Andean Amazon have also contributed. Merci à Mélanie Lemire et Myriam Fillion des jeunes chercheuses très inspirantes! I would like to thank Christian Abizaid and Chantalle Richmond for their excellent dissertations, which I made reference to innumerable times while structuring and formatting this dissertation.

I would also like to thank my parents who provided me with support and refuge when I have needed it. I write these words in loving memory of my dad who passed away in the first year of my doctoral studies. Dad, you’d be so proud of me. A special thanks to my mom who edited many parts of this dissertation. My work would not have been possible without the previous work I have done with my other supervisors: Timothy Johns, Vijay Aswani, Chandrasekhar and Meena Kanduri, Donna Mergler and Marc Lucotte. Nothing in my life is possible without the love and entertainment provided to me by my friends, Hiba, Freya, Ciara, Ann, Marlène, Anit, Ryan, Phil, Nico, and Pat. La famille de mon mari, Ginette, Claude, Marie-France, Stéphanie, Jonathan, Annabel, Zoé, Ron, Kiana and Noémie, ont aussi contribué à ma qualité de vie- surtout, Gigi, ma belle mère, qui s’est occupée de notre fils de façon régulier et attentionné pendant les deux dernières années de mon doctorat. I would like to acknowledge the role that yoga has played in giving me focus, mindfulness and joy and thank my teachers at the Sattva Yoga Shala, as well as Pattabhi Jois, the founder of Ashtanga yoga. A special thanks to Darby for all your guidance.

Finally, my new nuclear family is my ultimate inspiration. My husband, Nicolas Mainville, who I married in the first year of this journey, has not only been my partner in life but also an indispensible collaborator on this research. He continues to be my inspiration, forever pushing me to be a better person. The wellspring of my dedication to the environment comes from my commitment to future generations. My son, Joakim Dayton Mainville, and the new one on the way: this is for you.

vii Table of Contents Abstract...... i Résumé...... iii Acknowledgements...... v Contributions to empirical chapters ...... xi List of Figures ...... xiii List of Tables ...... xiv

Chapter 1: Introduction ...... 1 1.1 Research Context ...... 1 1.2 Objectives ...... 4 1.3 Conceptual Framework...... 4 1.4 The study area – Environmental Determinants of Contamination and Social and Health Considerations ...... 5 1.5 Methodological Framework...... 10 1.6 Organization of the Dissertation ...... 15

Chapter 2: Literature Review: Ecosystem Approaches to Health and Land-Use Change ...... 19 2.1 Ecosystem Approaches to Health ...... 20 2.1.1 History of the Ecosystem Approaches to Health ...... 20 2.1.2 Conceptual Framework of the Ecosystem Approaches to Health...... 22 2.1.3 Ecosystem Approaches to Health Methodology...... 26 2.1.4 An Ecosystem Approaches to Health Perspective Applied to the Current Study ...... 28 2.1.4.a Impacts of Land-Use Change on Local Communities ...... 29 2.1.4.b Impacts of Mercury Contamination on Local Communities 33 2.1.4.c Impacts of Petroleum Exploitation on Local Communities.. 35 2.2 Land-Use Change...... 39 2.2.1 Land-cover Change in the Andean Amazon...... 40 2.2.2 Land-use Change in the Andean Amazon ...... 42 2.2.2.a Agriculture...... 42 2.2.2.b Logging...... 43 2.2.2.c Non-Timber Forest Products (NTFP)...... 44 2.2.2.d Mining...... 44 2.2.2.e Conservation, Ecotourism and Environmental Services...... 45 2.2.3 Drivers of Land-use Change ...... 46 2.2.3.a Population Growth...... 47 2.2.3.b Poverty...... 48 2.2.3.c Roads and Market Integration...... 48 2.2.3.d Out-migration...... 49 2.2.3.e Soil Fertility...... 50 2.2.3.f Land Tenure...... 50 2.2.3.g Market Prices...... 51 2.2.3.h Governments...... 51 2.3 Conclusion ...... 53

viii Chapter 3: Comparison of Mercury in Ichtyofauna along Three Rivers of the Andean Amazon (Ecuador and Peru) ...... 54 3.1 Introduction...... 54 3.2 Methods...... 57 3.3 Results...... 59 3.3.1 Descriptive Statistics...... 59 3.3.2 Mercury Concentrations in Trophic Guilds ...... 60 3.3.3 Mercury Concentrations in Hoplias malabaricus...... 65 3.3.4 Mercury Concentrations in Hoplias malabaricus on the Napo River . 67 3.4 Discussion ...... 74 3.5 Implications...... 79

Chapter 4: Methylmercury in Hair of Riverine Populations along Three Rivers in the Andean Amazon (Ecuador and Peru)...... 81 4.1 Introduction...... 81 4.2 Methods...... 84 4.3 Results...... 88 4.3.1 Hair-mercury Concentrations in the Study Population...... 88 4.3.2 Change in Hair-mercury Concentrations in Residents of a Village with Increased Work Opportunities over the Period 2002-2006 ...... 99 4.3.3 Perception of Quality of Fish...... 103 4.4 Discussion ...... 104 4.5 Implications...... 110

Chapter 5: Mercury Concentrations in Urine of Riparian Communities Living Near Oil Fields in the Andean Amazon (Peru and Ecuador)...... 112 5.1 Introduction...... 112 5.2 Methods...... 117 5.3 Results...... 121 5.4 Discussion ...... 128 5.5 Implications...... 136

Chapter 6: Levels of 1-Hydroxypyrene in Urine of People Living in an Oil Producing Region of the Andean Amazon (Ecuador and Peru) ...... 137 6.1 Introduction...... 137 6.2 Methods...... 142 6.3 Results...... 146 6.3.1 Hydrocarbon Pre-health Outcome: 1-OHP Levels in the Study Population ...... 146 6.3.2 Hydrocarbon Health Outcome: Miscarriages in the Women of the Study Population...... 155 6.4 Discussion ...... 155 6.5 Implications...... 163

Chapter 7: Participatory Research and Dissemination of Research Results: The Use of Theatre and Videography ...... 165 7.1 Introduction...... 165

ix 7.1.1 Performance Arts in Health Research...... 165 7.1.2 Multiple Contaminants: An Environmental Health Issue of Importance in the Andean Amazon ...... 167 7.1.3 Dissemination Strategies and Mercury Research...... 168 7.1.4 Caution in Mercury Knowledge Transfer: Lessons Learned from the Inuit and Cree...... 171 7.2 Methods...... 175 7.2.1 Research to Action Challenge 1 – The Use of Theatre and Video in Knowledge Transfer among Amazonian Riparian Populations...... 177 7.2.2 Research to Action Challenge 2 – Endorsement of Sustainable Agricultural Practices among Small Land Holders...... 189 7.2.3 Research to Action Challenge 3 – Linking with Policy Makers...... 190 7.2.4 Research to Action Challenge 4 – Corporate Responsibility...... 190 7.3 Discussion and Conclusions ...... 191

Chapter 8: Conclusions...... 197 8.1 Chapter Summaries...... 198 8.2 Key Findings...... 206

Appendix 1: Questionnaire ...... 209 Appendix 2: Mercury Levels in Resident, Predatory, Amazonian Fish Species and Comparison with Results of Previous Studies ...... 217 Appendix 3: Reported Concentrations of Mercury in Urine of Populations from the Amazon and Andean Foothills...... 224 Appendix 4: Reported Concentrations of 1-OHP in the Literature ...... 225 References...... 227

x Contributions to empirical chapters

This dissertation is organized into chapters. In this section, I outline my own contribution and the contribution of others to the research. I designed each of these studies, gathered the data, performed much of the lab analysis, carried out the statistical analysis, interpreted the data and wrote the chapters. My supervisor (Oliver Coomes) and committee members (Nancy Ross and Donna Mergler) provided advice and/or assistance on all of the chapters. Other people also contributed through advice.

Chapter Three: Comparison of Mercury in Ichtyofauna along Three Rivers of the Upper Amazon (Ecuador and Peru) I performed all of the lab analysis on the fish samples. Nicolas Mainville helped with the sample collection of fish, informal interviews with fisherman, and provided comments on several drafts of the chapter. Charles Deblois, of UQAM, provided insight on the statistical analysis. Oliver Coomes provided comments on drafts of the chapter.

Chapter Four: Methylmercury in Hair of Riverine Populations on Three Rivers in the Andean Amazon (Ecuador and Peru) I performed all the lab analysis on the hair samples. Donna Mergler provided insight on sampling before the research was conducted. She also made contributions to structuring the statistical analysis. In addition, she made editorial comments. Oliver Coomes helped to determine how to structure and which variables to include in the clustered linear regression and made contributions through editing. Sébastian Breau provided advice on the clustered linear regressions.

xi Chapter Five: Mercury Concentrations in Urine of Riparian Communities Living Near Oil Fields in the Andean Amazon (Peru and Ecuador) Analysis of inorganic mercury in urine samples was performed at the First Nations and Inuit Health Branch Laboratory (FNIHBL), Health Canada in Ottawa using cold vapour atomic fluorescence spectrometry (CVAFS) by a lab technician. Creatinine analysis was carried out at the Centre de Toxicologie du Québec (CTQ) of the Institut national de santé publique du Québec (INSPQ) by a lab technician. Donna Mergler provided insight on sampling before the research was conducted. She also helped explore the data at the beginning of the statistical analysis. Oliver Coomes helped to determine which variables to include in the clustered linear regression and made editorial contributions. Sébastian Breau provided advice on the clustered linear regressions.

Chapter Six: Levels of 1-Hydroxypyrene in Urine of People Living in a Region of the Andean Amazon Contaminated by Crude Oil Analysis of 1-Hydroxypyrene in urine samples was performed at the First Nations and Inuit Health Branch Laboratory (FNIHBL), Health Canada in Ottawa using cold vapour atomic fluorescence spectrometry (CVAFS) by a lab technician. Creatinine analysis was carried out at the Centre de Toxicologie du Québec (CTQ) of the Institut national de santé publique du Québec (INSPQ) by a lab technician. Donna Mergler helped explore the data at the beginning of the statistical analysis. Oliver Coomes helped to determine which variables to include in the clustered linear regression and made editorial contributions. Sébastian Breau provided advice on the clustered linear regressions.

Chapter seven: Participatory Research and Dissemination of Research Results: the Use of Theatre and Video Oliver Coomes made contributions to this chapter in suggesting the integration of information on previous dissemination strategies used in mercury research.

xii List of Figures Figure 1.1: Map of the study area ...... 12 Figure 2.1: An "onion skin" diagram with nested hierarchies ...... 24 Figure 3.2: Box plot displaying Hg concentrations (μg/g, wet weight) on a log scale according to feeding regime...... 64 Figure 3.3: Hg concentration (μg/g, wet weight) vs. weight (g) on log scales for Hoplias malabaricus in the three regions ...... 68 Figure 3.4: Hg concentration (μg/g, wet weight) of Hoplias malabaricus in two villages of the Napo region ...... 70 Figure 3.5: Weight (g) of Hoplias malabaricus in two villages of the Napo region ...... 71 Figure 3.6: Hg concentration (μg/g, wet weight) vs. weight (g) of Hoplias malabaricus in two villages of the Napo region (Añangu (+) and Pañacocha (x)) ...... 72 Figure 4.2: Hair-mercury concentrations (μg/g) by river basin and community.. 92 Figure 4.3: Daily mercury intake (μg/day) by river basin and community ...... 95 Figure 4.4: Hair-mercury concentrations in the years 2002 and 2006 in 10 matched residents of the community of Añangu, Ecuador ...... 101 Figure 4.5: Hair-mercury concentrations in 2006 in residents of the community of Añangu, Ecuador, who had remunerated work (Hotel) and those who did not ...... 102 Figure 5.2: Mercury concentrations in urine (μg/g creatinine) by river basin and community ...... 125 Figure 5.3: Concentration of mercury in urine (μg/g creatinine) of women who use surface water for daily tasks vs. those who use wells, springs or rain water ...... 131 Figure 5.4: Mercury concentrations in urine (μg/g creatinine) in men who worked cleaning up an oil spill vs. those who held other positions.. 132 Figure 6.2: 1-OHP concentrations (μmol/mol creatinine) by river basin and community ...... 149 Figure 7.1: Mr. Mainville and Dr. Quizhpe helping a community member of Añangu, Ecuador, become an oil well ...... 180 Figure 7.2: Community member cutting down a tree in the play performed in San Carlos, Ecuador...... 182 Figure 7.3: A fish fight between a palometa and a fasaco in Palma Roja, Ecuador ...... 183 Figure 7.4: A bagre in Añangu, Ecuador, with a lot of mercury ...... 184 Figure 7.5: A fisherman in Añangu, Ecuador ...... 186 Figure 7.6: A woman from Añangu, Ecuador, fetching water in the river ...... 187 Figure 7.7: Mr. Mainville playing the role of fisherman in the game played in Palma Roja, Ecuador...... 188

xiii List of Tables Table 3.1: Mercury concentrations (μg/g, wet weight) in 30 fish species (422 fish) collected from the Corrientes (C), Napo (N) and Pastaza (P) regions...... 61 Table 3.2: Percentage of sampled fish exceeding the WHO safety recommendation (0.5 μg/g, wet weight) by river and by trophic guild . 63 Table 3.3: Regression model of log mercury concentrations in Hoplias malabaricus, wet weight (μg/g), Andean Amazon...... 66 Table 3.4: Regression equations and R2 for log Hg concentration (μg/g, wet weight) in Hoplias malabaricus from three regions of the Andean Amazon...... 69 Table 3.5: Regression equations and R2 for Hg concentration (μg/g, wet weight) in Hoplias malabaricus from two communities on the Napo River, Ecuador...... 73 Table 4.1: Characteristics of the study population by river in the Andean Amazon ...... 89 Table 4.2: Mean hair-mercury concentration (μg/g), number of fish meals per week, mean weight of fish caught in location (g), class of fish most commonly eaten (%), and mean daily Hg intake (μg/day) in the three rivers and eight communities ...... 94 Table 4.3: Total hair mercury concentrations (μg/g) (log-transformed data) and covariates in the Andean Amazon ...... 97 Table 4.4: Daily Hg intake (μg/day) and covariates in the Andean Amazon ...... 98 Table 4.5: Matched Pairs analysis of hair-mercury concentrations (μg/g), number of fish meals per week and weight of most commonly eaten fish for 2002 and 2006, Añangu, Ecuador...... 100 Table 5.1: Characteristics of the study population by river and sex in the Andean Amazon: age, ethnic group, schooling, alcohol use and smoking status...... 122 Table 5.2: Mean U-Hg concentration, occupational characteristics and dietary characteristics of the study population...... 124 Table 5.3: Concentration of mercury in urine (log-transformed data) and selected covariates ...... 127 Table 5.4: Concentration of mercury in urine (log-transformed data) and selected covariates in women...... 129 Table 5.5: Concentration of mercury in urine (log-transformed data) and selected covariates in men ...... 130 Table 6.1: Characteristics of the study population by river and sex in the Andean Amazon: age, ethnic group, schooling, alcohol use and smoking status...... 148 Table 6.2: Mean 1-OHP concentration, source of water, commonly eaten fish and number of miscarriages in the study population ...... 150 Table 6.3: Levels of 1-OHP (log-transformed data) in urine and covariates in women:...... 152

xiv Table 6.4: 1-OHP concentrations in urine of women using different water sources (River vs. Other or Surface vs. Other) for different tasks...... 153 Table 6.5: Levels of 1-OHP (log-transformed data) in urine and covariates in men...... 154 Table 6.6: Number of miscarriages and covariates in women...... 156 Table 7.1: Location, date and participation at the six performances of our play 179 Table A1: Reported mercury levels (μg/g) in resident, predatory, Amazonian fish species...... 220 Table A2: Reported concentrations of mercury in urine in populations from the Amazon and Andean foothills...... 224 Table A3: Reported concentrations of 1-OHP in the literature: location of the study, type of exposure, study population, 1-OHP concentration and reference...... 225

Chapter 1: Introduction

1.1 Research Context The development of frontier regions is often heralded as a panacea for poverty and well-being. Yet, in some cases, natural resource extraction, which is the foundation of economic development in frontier regions, is accompanied by its own health and social problems. These adverse effects are often not shared equally among the population. This dissertation examines some of the negative impacts associated with the changing land use patterns that have accompanied development in the Andean Amazon. Significant reservoirs of crude oil were found under the Amazonian forests of Peru and Ecuador in the 1960s. Fifty years of exploration, extraction and exportation have left a legacy of contamination and ecosystem degradation. The fitness of fisheries in parts of the Amazon is being compromised by mercury, a toxic agent, which is released from soils upon the clearing of river-side plots and which is contained in petroleum and petroleum wastes. A myriad of other contaminants, including polycyclic aromatic hydrocarbons (PAHs), are released into aquatic ecosystems by petroleum extraction practices in the region. This research considers two ecological services that intact watersheds provide to riparian communities in the Andean Amazon – healthy fisheries and clean water for household use – and the impacts that oil extraction and deforestation are having on the ability of the ecosystem to maintain these services.

Driven by the accelerating transformation of land use in the humid tropics, studies addressing the impacts of deforestation on the geophysical, biological, social, economic and political systems of different Amazonian countries have been conducted to evaluate the risks of these rapid changes. Impacts include increased surface albedo and changes in local temperature (Sagan et al. 1979), new carbon sources and the elimination of natural carbon sinks (Woodwell et al. 1983), changes in evapotranspiration (Shukla and Mintz 1982), disruption of the water

cycle (Hutjesa et al. 1998), reduction in biodiversity (Pimm and Raven 2000), soil nutrient depletion and erosion (Mainville et al. 2006). A lesser known impact of deforestation is the contamination of aquatic ecosystems with mercury, which compromises the ability of the watershed to provide untainted fish to local riparian communities.

Soil erosion, provoked by deforestation, leads to the leaching of naturally occurring mercury (Hg) into Amazonian aquatic environments (Roulet et al. 1999; Roulet et al. 2000; Mainville et al. 2006). The old ferralitic soils of the Amazon basin have accumulated natural mercury for millions of years and, thus, generally have high mercury levels (Roulet et al. 1998a). Volcanic soils near the Andes, although younger, also have high levels of mercury (Mainville et al. 2006). Volcanically-derived mercury can travel great distances (up to 20 000 km in the case of large explosions such as Krakatau (1883 AD) and Tambora (1815 AD)); however, the majority tends to settle nearby (Schuster et al. 2002, p.2306) where it adheres to iron and aluminum complexes in the soil (Roulet et al. 1998b). Once in aquatic ecosystems, a substantial portion of this heavy metal can undergo methylation, carried out by bacteria living around macrophytes and in sediments (Guimarães et al. 2000a; Guimarães et al. 2000b; Mauro et al. 2001). Methylation facilitates the entry of mercury into the food chain, where it accumulates at higher trophic levels (Malm et al. 1995; Malm et al. 1997; Maurice-Bourgoin et al. 2000b; Castilhos et al. 2001). Epidemiological studies have associated fish consumption, mercury levels and neurological deficits in Amazonian riparian populations (for a review see Passos and Mergler 2009).

Road construction, undertaken by oil companies, has been pivotal in the deforestation of the Ecuadorian Amazon (Pichon 1997a). Whereas the dynamic between mercury contamination and deforestation has been documented, the contribution of the petroleum industry to aquatic mercury levels is poorly understood. Practices used in the region are considered to be substandard (Kimerling 1990; Martínez et al. 2007) and petroleum and production waters (a

by-product of the extraction process) are known to contain mercury and PAHs (Bloom 2000b; Wilhelm and Bloom 2000). Burning of fossil fuels is a major anthropogenic source of inorganic mercury to the atmosphere (National Research Council 2000; Menounou and Presley 2003). Petroleum companies routinely burn off excess gases released while drilling and occasionally burn off spilt petroleum (Kimerling 1993; Martínez et al. 2007). Studies in Kuwait, Spain, and Nigeria have shown widespread contamination of the atmosphere and local ecosystems by metals due to sabotage burning of oil wells and spills (Onwumere and Oladimeji 1990; Sadiq and Mian 1994; Al-Muzaini and Jacob 1996; Gundersen 1996; Perez- Lopez et al. 2006; Al-Hashem et al. 2007). PAHs accumulate in aquatic organisms (Kochany and Maguire 1994). They are known carcinogens (IARC 1983) and lead to adverse pregnancy outcomes (Detmar et al. 2006).

This dissertation assesses the levels of mercury in fish and human populations and PAHs in local communities along three rivers in the Ecuadorian and Peruvian Amazon. Changes in land use and deforestation in the three river basins differ substantially. The Napo River Valley, Ecuador, is considered one of the world’s 14 deforestation fronts, with a deforestation rate of 3.0% per year (Myers 1993, p.11). Although reliable statistics do not exist for the northern Peruvian Amazon, the two rivers under study here have been considerably less affected by deforestation than the Napo River. The Corrientes River has been a site of oil extraction since the 1970s, but since no roads were built to the region it exhibits very limited deforestation. Petroleum activities were responsible for the deforestation of only 427 ha in the region of the Corrientes studied here (Martínez et al. 2007, p.5) and little colonization has occurred. The upper reaches of the Peruvian Pastaza River touches the western limit of a petroleum concession active since the 1970s, but access to this oil field is attained via the Corrientes River. The lower parts of the Pastaza River are currently undergoing petroleum exploration. No roads connect it to commercial centres on the Peruvian side and very little deforestation has taken place. However, on the Ecuadorian side, closer to the Andes, a substantial amount of deforestation has occurred on the Pastaza

River. Indeed, a study examining the leaching of metals, including Hg, in the upper Pastaza (Ecuador), where the human population is dense and land clearing common, found high levels; downstream, however, these levels dropped markedly as tributaries diluted the concentrations (Saunders et al. 2007). Natural phenomenon, such as active meander plains, can also lead to forest loss (Puhakka et al. 1992), but the amount is insignificant in comparison to the deforestation occurring on colonization fronts.

1.2 Objectives The research objectives of this study are: 1. To determine the levels of mercury in commonly consumed fish species in the Andean Amazon. 2. To determine the levels of mercury in the hair and urine of rural populations living in socially and geographically contrasting settings of Andean Amazonia and to evaluate the environmental factors, particularly deforestation and oil extraction, contributing to this contamination. 3. To determine the levels of 1-hydroxypyrene in the urine of rural populations living in socially and geographically contrasting settings of Andean Amazonia and to evaluate the role of oil extraction in contributing to this contamination. 4. To examine the incidence of miscarriage in women of the study population in relation to levels of 1-hydroxypyrene. 5. To effectively communicate the results of the research to study participants, national government agencies, health care providers and non- governmental organizations.

1.3 Conceptual Framework The conceptual framework used is in this research is the ecosystem approaches to health (Forget and Lebel 2001) (described in Chapter 2). The complexity of and the role ecosystems play in maintaining global earth functions and human health are becoming increasingly apparent. The understanding of these relationships becomes enhanced as ecosystems research, traditionally pivoting around the biological sciences, is made transdisciplinary by integrating socio-economic, cultural, political, and health factors. The ecosystem approaches to health framework scrutinizes complex relationships further by considering gender differences and social equity. Since the exposure pathways in the current study population were expected to be different for women and men, the use of the

ecosystem approaches to health framework gave structure to this inquiry. The ecosystem approaches to health framework also stresses the importance of community participation in research. The dissemination component of this research was guided by a participatory approach.

1.4 The study area – Environmental Determinants of Contamination and Social and Health Considerations The research undertaken here aims to contrast the Napo River System, Ecuador, an area of intense oil extraction and deforestation, with the Pastaza River System, Peru, a region undergoing limited petroleum exploitation and which is experiencing an intermediate level of deforestation upstream and the Corrientes River System, a river system that has been heavily contaminated by petroleum waste products and spills, but which is without roads and large-scale deforestation. The three rivers form a continuum of deforestation intensity and contamination by petroleum activities. The Napo River, in Northern Ecuador, is born of three volcanoes – Cotopaxi, Antisana, and Sincholagua – in Ecuador, eventually becoming a meandering white water tributary of the Amazon River, downstream of Iquitos. The Pastaza River is created at the confluence of the three rivers flowing from the Chimborazo Volcano and the Curtuchi River, which has its wellspring at the Iliniza Volcano and flows over the Andean tableland for a hundred kilometres before plunging down into the Amazon. It passes through southern Ecuador and Northern Peru and then merges with the Marañón River. The Corrientes River is a lowland river that rises in the foothills of the Andes.

Soils. Studies on mercury, deforestation and health have focused, to date, on the Brazilian Amazon. The nature, pace and pattern of development in the Andean Amazon is distinct (discussed in Chapter 2) and the biogeochemical features of the environment are different from the lower lying basin in Brazil. Soil types determine the concentration of mercury and land-use patterns of local people. All three rivers examined in this research are situated in the Pastaza megafan and drain soils created from volcanoclastic debris (Harden 1986; Räsänen et al. 1992;

Willink et al. 2005; Mainville et al. 2006; Perrault-Archambault and Coomes 2008), primarily andisols, rich in mercury (Mainville et al. 2006) and easily erodible (Räsänen 1991); however, the tributaries of the Napo and the Pastaza rivers originate in the Andes whereas those of the Corrientes River do not. A study evaluating the mercury burden of soils along the Napo River showed that, in the Andean foothills, Hg concentrations varied from 2.9 mg/m2 at 0-5 cm to 11.2 mg/m2 at 25-50 cm (Mainville et al. 2006, p.94). Further from the Andes, where the soils are older, concentrations varied from 4.1 to 17.2 mg/m2 at the same soil depths (Mainville et al. 2006, p.94). This study also calculated an average loss of 2 2.2 mg/m of mercury upon deforesting (p.96). Even though the Andes is a major source of mercury to the region, older soils in Brazil have higher concentrations of mercury because they have had more time to accumulate mercury (Roulet et al. 1998b; Fostier et al. 2000).

Ecoregions. Mercury levels also can be altered by the extent and nature of the organic matter on the surface of the soil (Roulet et al. 1998b). Since the three river basins exist in the same ecoregion – the Napo moist forest ecoregion – the nature and extent of humus could be assumed to be similar, although no comparative studies are reported in the literature.

Water chemistry. The methylation of mercury is influenced by the acidity, organic matter content, and water flow velocity of Amazonian rivers (Guimarães et al. 2000a). Fish diversity also varies with water conditions such as substrate, turbidity and pH (Ibarra and Stewart 1989). All three river basins constituting the study area are white water rivers and the water chemistry of each is relatively similar. The Iquitos varzea ecoregion reaches up the river banks of the Pastaza and the Corrientes rivers. The region receives between two to four meters of rain per year and, whereas there are no marked wet and dry seasons, December to February is a relatively drier period and May and June are relatively wetter months. The waters of all three main rivers are neutral to alkaline although creeks tend to be slightly acidic (Pezo et al. 1987; Ibarra and Stewart 1989; Willink et al.

2005). Copious amounts of organic matter are found in these rivers and their associated creeks and lakes (Pezo et al. 1987; Willink et al. 2005). Suspended solids in streams of the Upper Napo attained values varying between 3 and 19.2 mg/L (Bojsen and Barriga 2002, p. 2260). Samples taken in the Pastaza River showed the dissolved organic carbon (DOC) to be between 150 and 200 μM/L (Briceno 2005, p.26). Close to Andoas, production waters from the petroleum companies bring turbid water with high conductivity and oxygen content into the Pastaza River (Briceno 2005). These values decrease with distance from Andoas (Briceno 2005). It could be assumed that this would be the case near most centres of petroleum activity. The water flow velocity of the Pastaza is between 0.6 and 2.4 m/s (Tapp 2007) and the water flow volume is 772-1077 m3/s (mean: 913 m3/s) (Martinez 2007, p.18). The water flow volume of the Corrientes River is less: 133-242 m3/s (mean: 180 m3/s) (Martinez 2007, p.18). In the Napo area, conductivity has been reported to be between 11-115 μS/cm (Bojsen and Barriga 2002, p.2260). The conductivity of the Pastaza and the Corrientes varies between 90-147 μS/cm (Pezo et al. 1987, ch.4.4).

Petroleum concessions. All three regions have been undergoing oil exploitation since the 1970s and could be considered extractive peripheries (Lobao and Brown 1998). Petroleum activity is concentrated around the town of Coca on the Napo River and in the Peruvian part of the Pastaza and Corrientes Rivers. Petroleum concession blocks, operated by at least 35 multinational oil and gas companies, now number around 180 and cover approximately 688,000 km2 of the western Amazon (Finer et al. 2008, p.e2932). Over two-thirds of the land area in both the Ecuadorian and Peruvian Amazon lie within these oil concession blocks (Finer et al. 2008, p.e2932). Lot 1AB, operated by PlusPetrol and located on the Corrientes and Pastaza rivers, accounted for the production of 24% of the total production in Peru in January 2005 (Gutierrez Choquevilca and Huboux 2006, p.2). Peruvian protected areas prohibit oil and gas activities, whereas until the new constitution was passed in 2008, Ecuadorian laws did not (Finer et al. 2008).

Contamination. In the last twenty years, the Ecuadorian Amazon has exported 1.5 million barrels of petroleum (Kimerling 1993, p.11) through a pipe-line traversing hundreds of kilometres of rugged Amazonian and Andean terrain (Barthélémy 2003). It is estimated that at each treatment facility in the Ecuadorian Amazon, 4.3 million gallons of liquid waste is generated every day (Hurtig and San Sebastián 2004, p.245). These wastes are held in open-pits without treatment, from which they are directly discharged into the environment, gradually leak into the water-table and/or occasionally spill over during periods of heavy rain (Hurtig and San Sebastián 2004). Estimates place toxic waste discharges at 5 million gallons per year, amounting to 30 billion gallons between 1967 and 1993, in the Ecuadorian Amazon through the routine maintenance activities of the petroleum companies (Hurtig and San Sebastián 2004, p.245). An estimated 762,000 barrels of production waters are produced per day in the boarder region of the Corrientes and Pastaza Rivers (block 1AB) and 183,000 barrels per day in the region of the Corrientes studied here (blocks 106 and 104) (Martínez et al. 2007, p.7). High levels of mercury were found in all rivers receiving production waters in northern Peru, including the Corrientes River and the Pastaza River (Martínez et al. 2007). A study in the Corrientes region showed that 34 ha surrounding petroleum activities were highly polluted with barium, another heavy metal hauled up in production waters, 95 ha were moderately polluted and 292 ha were slightly polluted (Martínez et al. 2007, p.5). In terms of atmospheric contamination, the approximation is that 1.5 million cubic meters of gas from the separation process are burned every day at each facility in the Ecuadorian Amazon, without any emissions or temperature control (Hurtig and San Sebastián 2004, p.245). In Block 1AB, 56.9 million cubic meters of gas were burned in 2005 (Martinez 2007, p.55).

Health. Studies in the Ecuadorian Amazon have shown that health impacts, such as headaches, diarrhoea, and skin, eye, nose and throat irritations, result from exposure to petroleum and petroleum wastes (Instituto de Epidemiología y Salud Comunitaria (IESC) "Manuel Amunárriz." 2000). Cancer incidence, including

cancers of the stomach, rectum, skin melanoma, soft tissue, kidney, cervix and lymph nodes, has also been shown to be elevated in exposed communities (San Sebastian et al. 2001a; Hurtig and San Sebastian 2002a; Hurtig and San Sebastian 2002b; Hurtig and San Sebastián 2004). Malaria and other vector borne diseases affect the population. Diarrhoea is a major health problem especially among children. Access to health services and dental care is difficult because of long distances and cost.

Diet. Most Amerindian groups in Amazonia fulfill energy requirements through cultivated carbohydrates, usually manioc, sweet potato, maize or banana/plantain. Groups tend to specialize in one, or perhaps two, starchy staples, in this case manioc and plantain, while other cultigens and wild plant foods contribute substantially to vitamin and mineral requisites (Milton 1991; Dufour 1992). These starch-based diets are poor in protein so animal flesh and/or fish are important supplements to attain adequate protein and fat allowances (Milton 1991). There is a great diversity of fish species in the Amazon and people eat a variety of fish including herbivores, piscivores, omnivores and benthivores. People in riparian communities eat up to seven fish meals per week (Webb et al. 2004) (see Chapter 4). Hunting has declined substantially in the Napo River basin due to high rates of deforestation, petroleum activities, overhunting, established settlements and restrictions imposed by conservation/ecotourism initiatives (Wunder 2000; Canaday and Rivadeneyra 2001; Franzen 2006). Hunting is also on the decline in the Corrientes and Pastaza River basins. Game, with the exception of fish eaters, does not biomagnify mercury in the same way that fish does, because mercury in the terrestrial environment remains in its elemental form.

Livelihoods. Livelihoods in the Andean Amazon are based primarily on subsistence agriculture, fishing and, to a lesser extent, hunting. Traditional communities practice shifting cultivation, whereby plots are left to fallow after several harvests (Denevan 1980). Cattle ranching is popular among colonists in the Napo River basin (Pichon 1997a). Communities closer to markets have both greater access to remunerated work and market goods. The petroleum industry

offers contract work or shift work (28 days in, two weeks out) to men in communities close to wells in the Peruvian Amazon. However, in the Ecuadorian Amazon, companies have tended to rely more on migrant workers, primarily from the Andes. Work in the tourism industry is an option for people from some communities located near hotels and parks.

1.5 Methodological Framework The use of the ecosystem approaches to health conceptual framework provided a heuristic guide to the research in which: (1) the problem was defined in transdisciplinary terms with community member input and reference to the literature; (2) an exposure pathway (fish) was measured; (3) three bioindicators of contamination in humans were determined (hair-mercury, urine-mercury, and 1- hydroxypyrene (1-OHP)); (4) one human health outcome was evaluated (miscarriages); and, (5) the results were shared with participants in an engaging way. A hypothesis-driven study design with purposefully chosen study sites was employed in order to conduct this natural experiment. A mixed methods approach was used in carrying out the research. The hypotheses were that there would be (1) higher levels of mercury in fish from more deforested regions; (2) higher levels of mercury in the hair of populations that consumed more fish; (3) higher levels of mercury and 1-OHP in the urine of people more exposed to contamination from the petroleum companies; (4) a greater number of miscarriages among women more exposed to contamination from the petroleum activities; and, (5) that theatre would be a successful way of engaging participants in the dissemination process.

The three river basins were chosen because of the gradient in petroleum exploitation/deforestation. The Napo River system in the Ecuadorian Amazon is undergoing oil exploitation and rapid deforestation, whereas the Pastaza River system, in the Peruvian Amazon, has been exploited for oil during a similar time period in only the upper reaches, and, likewise, has experienced deforestation only upstream. The Corrientes River system, Peru, is heavily contaminated by

hydrocarbons and little deforested. One of the principal differences between these river systems is the construction of roads in Ecuador, but not in Peru, where operations are conducted via river or air.

The field component of this research involved three trips to the study area. A reconnaissance trip was made to the Pastaza River in early 2006 to determine if the land-use characteristics in the region were suitable for the study. The sampling was carried out during a subsequent trip between July and December 2006. The questionnaires were administered and samples taken in three communities along the Napo River (Palma Roja, Añangu, and San Carlos), three along the Corrientes River (Peruanito, Copal, and Nuevo Paraiso) and two on the Pastaza River (Alianza Capuhauri and Loboyacu) (see Figure 1.1). The results were returned to the communities on the Napo River and the Pastaza River and community leaders of the Corrientes River in 2009. For the sampling field trip, the team consisted of the author, Nicolas Mainville (biologist) and Edy Quizhpe (medical doctor) in Ecuador and the author, Nicolas Mainville (biologist), Carlos Rengifo (field assistant) and José Yacum (field assistant) in Peru. For the research results dissemination, the team consisted of the author, Nicolas Mainville (narrator) and Edy Quizhpe (narrator) in Ecuador and the author, Nicolas Mainville (narrator) and Mauricio Delfin (video director) in Peru.

Figure 1.1: Map of the study area

The primary intention of this research was to assess pre-health outcomes: bioaccumulation in fish and concentrations of Hg and 1-OHP in humans. A well defined clinical diagnosis of mercury poisoning requires clinical testing, since the health outcomes are subtle. The primary health outcome of exposure to PAHs – cancer – would have been equally difficult to evaluate. Respondents were not able to distinguish whether they or someone in their family had had cancer since medical attention in the area is limited. One health outcome of exposure to hydrocarbons was captured in this research: miscarriages. Most women were able to report on the number of miscarriages they had experienced. This health outcome is examined in relation to the hydrocarbon pre-health outcome.

In order to capture maximum fish consumption, sites were selected from among the smaller, indigenous villages (~50-200 adults) of each river system, since larger communities tend to keep more domestic animals and indigenous people tend to eat more fish than mestizos living in colonist communities. Selection among these villages was based on logistical considerations (distance, available transportation, etc) and on their willingness to participate. In all but one case (San Carlos, Ecuador), the communities are reachable only by river. Permission to work in the community was obtained from the village Apu – the elected community leader – and the Teniente Gobernador – the government representative. Once the appropriate local officials had granted permission, a village meeting was held to discuss the project. A consensus was then reached as to whether the community would grant permission to carry out the work. Each individual of the community was visited at his or her house for the sampling. All adults were eligible and all potential participants could decide to withdraw at any moment. No compensation was provided. An ethics certificate for this study design was obtained from the McGill University Ethics Review Board.

If informed consent was provided, questionnaires were administered. The questionnaire (see Appendix 1) was validated for cultural context in a previous study in the region (Webb et al. 2004). The questionnaire consisted of

approximately 35 short questions organized into five sections – personal information (age, sex, ethnic group, number of children, etc.), health (smoking, drinking, health problems), occupation, fishing, and diet (including water). The questionnaire took approximately a half an hour to complete. Since mercury and PAH exposure was hypothesized to be partly a result of the type and amount of fish eaten, diet questions focused on the frequency (number of times per week), species and provenance (location of fishing) of fish consumed. Since exposure via water was also a hypothesis, questions on the source of drinking and washing water were asked. Finally, since the type of work individuals carry out can also lead to exposure, questions on work in artisanal gold mining and with petroleum companies were posed. Three open-ended questions to respondents addressed changes in fish quality and quantity: Have you noticed any changes in the fish in recent years? In comparison with 10 years ago, is the fishing better, worse or the same? In your opinion, why is this? In comparison with 10 years ago, do you eat more, less or the same amount of fish? Why is this? Ten years was chosen as a reference point to capture long-term trends in diet. The questionnaire was adapted from the one used by researchers at UQAM and McGill University (Legrand 2005). The questionnaire was translated into Spanish by the author and verified by two Spanish speakers (Edy Quizhpe and Carlos Rengifo). The questionnaires were administered by the author and her assistant, Carlos Rengifo. Five focus groups were performed to help inform the research and validate the questionnaires.

A small locket of hair from each participant was cut at the root from the occipital region of the head. The hair sample was stapled at the base and stored in plastic, Ziploc™ bags, until analysis. A subsample of informants was asked to urinate into a cup in private as a single void. Approximately 40ml was taken – 20ml for the 1- hydroxypyrene analysis and 20ml for the inorganic mercury analysis. The cup was labelled and frozen in a kitchen-style freezer (approximately -4-0°C) until returning to Canada at which point it was kept in a laboratory freezer (approximately -20°C). Urine sampling is preferable to blood sampling, as urine is

less invasive and commonly taken in the Western Amazon for other health interventions.

Fishers were approached in each village and asked for a small sample of their catch. Sampling of fish was not random, but attempted to represent as many consumed fish species as possible by excluding fish that are not consumed and by sampling fish brought back to families’ kitchens. Two additional sampling sites were added on the Napo River (Pañacocha and Coca) because fishing is less frequent on the Napo River (see Figure 1.1). Fish were identified, measured and weighed. Less than 10g of flesh was cut from the tail muscle. Samples were placed in Nalgene™ scintillation vials and frozen until analysis. While sampling fish, informal interviews about fish ecology and fishing lore were conducted to identify species and trophic level.

1.6 Organization of the Dissertation This dissertation was written as a series of chapters intended for publication in scientific journals once modified. The heuristic of the research methodology formed the basis for the organization of the dissertation: beginning with an examination of the multiple factors influencing the current situation (Chapter 2), evaluating a source of human exposure to contamination (fish) (Chapter 3), progressing through with the measurement and analysis of the levels of contamination in humans (Chapters 4 (hair-mercury), 5 (urine-mercury), and 6 (1- OHP)), and concluding with an intervention to improve human health (Chapter 7).

Chapter 2 reviews the scientific literature on the theoretical framework used to conceptualize the environmental health problem addressed in this dissertation: ecosystem approaches to health. The section on the ecosystem approaches to health discusses the history, theory and methodology of the framework before applying some of the principals to three of the important changes taking place in the study area: land-use change, mercury contamination and petroleum extraction. A section on land-use change examines the literature specific to the study region

in order to pinpoint some of the upstream causes of environmental change. The similarities of these two distinct fields are highlighted and the merits of using the two simultaneously are argued.

Chapter 3, the first empirical chapter, examines the issue of mercury in fish and the potential risks to fish consumers. Data on mercury levels in fish specific to this region of the Andean Amazon is lacking. Further, comparisons across rivers can lead to discoveries about the sources of contamination. In this chapter, the relevant literature is reviewed. The levels of mercury found in fish samples are then presented according to species and trophic level. Linear regression techniques are used to analyse the data from a non-migratory, predatory fish species (Hoplias malabaricus) and to draw conclusions about the rate of mercury bioaccumulation in the three river basins. Differences in the rate of bioaccumulation are discussed in light of the land-use changes taking place along the rivers and the extent of pollution from the petroleum industry.

Chapter 4 examines mercury contamination in human hair from populations of the study region. First, the literature on organic mercury levels in Amazonian populations and health impacts is reviewed. The chapter uses data from the analysis of mercury in human hair and from questionnaires conducted with participants to examine human exposure to mercury and links to diet. Data on mercury levels, amount of fish consumed and type of fish preferred are presented for each river. Regression techniques are then used to examine the socio- demographic differences in the observed mercury levels and differences related to diet. Qualitative data from the questionnaires assess perceptions of the quality of fisheries. How these perceptions differ between communities is explored. The discussion focuses on the consequences of mercury contamination in the diet for local people.

Chapter 5 examines inorganic mercury contamination in human populations from the study region. The corpus of literature on inorganic mercury is distinct from

that of organic mercury and is reviewed in the introduction to this chapter. The geographic variations in inorganic mercury levels in urine are described for the study population. Relying again on the questionnaire data, the links between sex, occupation, diet, and socio-demographic variables and mercury levels are examined. Regression analysis stratified for sex explores the factors associated with inorganic mercury levels. The Discussion makes links between the observed levels of inorganic mercury, occupation and source of water.

Chapter 6 addresses another contaminant found in the mixture created by petroleum extraction: PAHs. A review of the literature on PAHs, pyrene (one of the PAHs) and 1-hydroxypyrene, a metabolite of pyrene, is presented. Descriptive statistics illustrate the extent of pyrene contamination in the study populations from each river. Stratified linear regressions assess which variables are associated with observed 1-hydroxypyrene levels for men and women. It is in this chapter that the one human health outcome is considered. Number of miscarriages in 26 women was examined in relation to levels of 1-OHP while controlling for age using linear regression. The Discussion makes links between the results on the pre-health outcome (1-OHP exposure pathways) and the health outcome (miscarriages).

Chapter 7 describes the dissemination of research results among study participants through performance arts, specifically, theatre. In the introduction to this chapter three bodies of literature are explored. The nascent body of literature on the use of performance arts in health research is examined. Other communication strategies used in mercury research are then presented. Finally, the failure of mercury research communication in the Canadian North is discussed. The play is then described in detail with reference to photos of several of the performances. The lessons learned and the ways in which this activity could have been evaluated are examined in the Discussion.

The final chapter, Chapter 8, summarizes the conclusions from each empirical chapter. The substantive and methodological contributions of the findings to academic scholarship are discussed and the limitations of the analytical approaches used in the research are delineated. Finally, the most salient policy recommendations stemming from the findings are summarized.

Chapter 2: Literature Review: Ecosystem Approaches to Health and Land-Use Change

The field of ecosystem approaches to health explicitly explores the interactions among ecosystems, social systems and human health. One environmental disruption increasingly singled out by ecosystem approaches to health research is deforestation and land-use conversion. Researchers studying land-use and cover change (referred to by some as LUCC) have undertaken the daunting task of describing and quantifying the extent of changes taking place in people’s use of their territory and consequent land surface changes. The causes of the changes in land use that have occurred in recent centuries are also explored. The land-use change literature occasionally highlights the impacts of these changes on ecosystems and local populations, although this has not been the central focus of research.

Land-use change research and ecosystem approaches to health are distinct paradigms that examine the problem of deforestation and land-use conversion from different angles. Yet the two approaches are founded on similar principles. Both are concerned with upstream causes. Both recognize that there are complex webs of interactions – physical, economic, political and social – involved in the problems. Both integrate ideas of empowerment and equity at the individual and household level with the environmental communities’ concerns about the impacts of human land use at the local and global scale. For example, combining agent based perspectives with a narrative and systems approach unearths a myriad of underlying causes of land-use change (Lambin et al. 2003). Finally, research from both fields is increasingly making use of mixed methods, i.e. integration of household survey data and satellite data or social network data and contamination levels. The two conceptual frameworks can inform each other and be used alongside one another to build a comprehensive and holistic picture that describes the nature of the changes taking place, the causes and the impacts.

In this chapter, the growing body of literature on ecosystem approaches to health is reviewed. As part of this section the ecosystem approaches to health is applied to the current case study by looking at the larger health impacts of land-use change, mercury in fisheries and petroleum exploitation. In the second section, the literature on land-use change in Peru and Ecuador is explored. Finally, theories explaining the underlying drivers of land conversion are discussed.

2.1 Ecosystem Approaches to Health

The objective of the ecosystem approach to human health is to enhance the health of communities by instituting ecosystem- management methods that will foster the sustainability of the ecosystem itself and the health of the human beings who are part of it. (Forget and Lebel 2001, p.S29)

2.1.1 History of the Ecosystem Approaches to Health The ecosystem approaches to health is an emerging field that bridges disciplines to situate human health in the context of the physical and human environment (Forget and Lebel 2001). In this framework, the politico-economic, socio-cultural, and biogeochemical factors which converge to influence human health are taken into consideration. The definition of health used in the ecosystem approaches to health is broad and akin to that used in the 1946 preamble to the constitution of the World Health Organization (WHO), which defines health as “a state of complete physical, mental and social wellbeing and not merely the absence of disease or infirmity” (p.1). This definition was further refined by the WHO to include concepts of capacity and resilience: health is “the extent to which an individual or a group is able to realize aspirations and satisfy needs, and to change or cope with the environment” (WHO 1984, p.4). In this definition, health is not only an end in and of itself, but also a means to attaining goals.

The ecosystem approaches to health draws upon a variety of paradigms, including complex systems analysis, community engagement, and gender and equity

analysis. It is also closely allied with similar conceptual frameworks, such as sustainable development and integrated resource management. The social determinants of health and la medicina sociale are similar frameworks, but with less emphasis on environmental deterioration. Some people have referred to the ecosystem approaches to health as eco-social or adaptive management approaches (Waltner-Toews and Kay 2005); others have used the term EcoHealth (Lebel 2003). The term “ecosystem approaches” was first used in 1978 in a report to the International Joint Commission from the Great Lakes Research Advisory Board [now the Great Lakes Science Advisory Board] (GLRAB 1978). The report argued that water could not be adequately managed by considering water alone (Vallentyne and Munawar 1993). This report heralded a significant shift in thinking about water management across political boundaries. The conceptual framework was further elaborated by Allen et al. (1993), also in the context of Great Lakes Management. James Kay brought his background in physics to the field by introducing ideas of thermodynamics and complex systems thinking (Kay et al. 1999). He elaborated “the diamond schematic,” which is a Venn diagram where the needs of the ecosystem overlap the needs of the society in the presence of policy makers and managers (Kay et al. 1999). These early approaches were primarily concerned with healthy ecosystems (Rapport 2000); however, beginning to view ecosystems in terms of human health provided important opportunities for the integration of social and health sciences into environmental management (Rapport et al. 1998). Further, ecosystem health was beginning to be linked to the services that ecosystems provide human communities to sustain them (Rapport et al. 1998).

Meanwhile, several ecologic approaches to human health that considered four determinants of health – environmental, social, lifestyle and genetic – were evolving (Forget and Lebel 2001). This movement was built on a broader evolution of the concept of health toward a more comprehensive and holistic vision (Lalonde 1974; WHO 1986). The use of the term ecosystem approaches to human health was first introduced in the late 1990s by Forget (1997) and was an

attempt to integrate ideas from new developments in ecosystem health with ecologic approaches to human health. Applying the term ecosystem approaches specifically to human health responded to growing dissatisfaction with using particular disease outcomes as the basic indicators of health (Waltner-Toews and Kay 2002). The International Development and Research Centre (IRDC) has been an active champion of the ecosystem approaches to health. The IDRC hosted the first International Forum on Ecosystem Approaches to Health, in Montreal, May 18– 23, 2003 at the University of Québec at Montréal. The IDRC supports research projects using the ecosystem approaches to health across the globe and funds several regional Communities of Practice in EcoHealth.

There continues to be a distinction made between ecosystem health and ecosystem approaches to health, although some claim that this is semantic (De Plaen and Kilelu 2004). DePlaen and Kilelu (2004) write, “Ecosystem Health adopts a lens that emphasizes the importance of achieving a healthy ecosystem as a condition to good human health, whereas Ecohealth emphasizes the potential of ecosystem management to improve the health of human populations” (p.9). In any scenario, researchers and practitioners are increasingly of the opinion that there are important linkages between human health and ecosystem health and that the influences are bidirectional (Rapport 2000).

2.1.2 Conceptual Framework of the Ecosystem Approaches to Health The ecosystem approaches to health, as elaborated by the IDRC, has traditionally included three pillars: transdisciplinarity, social justice and gender equity, and stakeholder participation (De Plaen and Kilelu 2004). Recognizing that health is contingent on the biophysical, social, economic and political environment necessitates an approach that transcends disciplines. One of the central characteristics of this approach is that it considers the health of a person or population to rest inside a set of nested hierarchies all of which are imbedded in the biosphere (Nielsen 2001). These hierarchies represent the physical,

sociocultrual and political environments within which the person or population lives. Several visuals of this hierarchy have been proposed. Mergler developed what is referred to as the “onion skin” diagram (see figure 2.1) (Mergler, unpublished). The ecosystem approaches to health also recognizes that systems – be they human or ecological – are inherently uncertain and complex and that there is profound interconnectedness between elements of the system (Nielsen 2001). Further, influence can flow in both directions: an individual’s health can be affected by the physical environment, but the ecosystem’s health can also be impacted by the activities of the individual (Waltner-Toews and Kay 2005). The use of transdisciplinarity has also been referred to as a “new integrative science” (Rapport et al. 1998).

A second crucial element of the ecosystem approaches to health is gender and social equity. In most cultures there are stark differences in the roles, responsibilities and health status of men and women. Roles and responsibilities lead to different exposure pathways and risks for men and women, and disparate health status results in differing vulnerability. There are important biological differences, related to factors such as reproduction and metabolism, that interface with exposure to contaminants and other health risks. Further, men and women relate to their environment in different ways, leading to different exposure pathways and perceptions of risk. Globalization and structural adjustment may affect men and women differently, increasing exposure for some and not others (London et al. 2002). Finally, many women work in the informal sector and their exposure or risk might not be fully recognized (London et al. 2002). In many societies, ethnicity or caste are also important determinants of health (Forget and Lebel 2001). Social status often defines a group’s exposure pattern through, for example, which work they do or where they live, but it also establishes access to resources. A group with less access to food, clean drinking water, health care, medicine, support structures, and secure living environments will be more vulnerable to the same environmental hazard as a group with greater access. A further consideration is a group’s control over resources (Forget and Lebel 2001).

Figure 2.1: An "onion skin" diagram with nested hierarchies (Mergler, unpublished).

For example, women may have access to health care, but no control over the type of service they receive. EcoHealth studies are designed such that social variables, such as sex, caste, ethnic group, etc, are differentiated. This is important not only for the validity and accuracy of our understanding of the science but also to generate solutions that will be appropriate for and geared to the exposure routes and vulnerabilities of each social group. Finally, different sectors of the population face different barriers to participation and might require different conditions for participation (Mertens et al. 2005).

A third underlying principle of the ecosystem approaches to health is participation. Genuine contributions from stakeholders – such as policy makers and local residents – in all phases of the research process, is a hallmark of the ecosystem approaches to health. The first step of the cyclical process of participatory research is inquiry (Mertens et al. 2005). Integrating local people in this phase is important in identifying problems which are a priority to them (Forget and Lebel 2001). The second step is reflection: participants are called upon to add their perspective and interpret the situation (Mertens et al. 2005). The final stage in participatory research is action (Mertens et al. 2005). Local support is important when designing interventions that will be accepted by end-users (Forget and Lebel 2001). The ecosystem approaches to health benefits from the contribution of as many stakeholders as possible but rallying support for and participation in the research is one of the greatest challenges of this approach (Waltner-Toews and Kay 2005). Who ends up contributing can change the outcomes of participatory research (Mertens et al. 2005). A research activity that does not include a cross-section of the population can contribute to inequity in the community (Mertens et al. 2005). Involving stakeholders in the research process has led to the ecosystem approaches to health being referred to as democratic and/or participatory science (Waltner-Toews and Kay 2002). Participatory research leads to the understanding that: any complex system is subject to interpretation from different legitimate perspectives and, hence, that problem resolution cannot depend only on objective technical or scientific expertise. Rather,

drawing on various bodies of accepted knowledge, stakeholders must negotiate a continuing series of resolutions within basic ecological constraints. Thus, sustainability does not result from adopting a package of technologies and practices, but from establishing a process of learning and investment in local governance. (Waltner- Toews and Kay 2002, p.16)

2.1.3 Ecosystem Approaches to Health Methodology The ecosystem approaches to health purposefully uses the plural of “approaches” to avoid being prescriptive (Waltner-Toews and Kay 2005). The intent of this conceptual framework is to outline guiding principles. The study design is informed by these guiding principles as well as the appropriate methodology necessary to meet the specific research objectives. A combination of quantitative and qualitative inquiry and analytical methods gives the richest picture of the situation (Waltner-Toews and Kay 2005). Qualitative methods, such as focus groups and interviews provide crucial information and give insight into the perceptions and feelings of stakeholders (Mertens et al. 2005). A study of the historical context has been recommended (CSDH 2008). Traditional epidemiological, biological and statistical analytical methods also have their place in ecosystem approaches to health work. An emerging technique is the use of narratives to generate community participation (Waltner-Toews and Kay 2005). Combining all of these research methods is not often feasible, but integrating the guiding principles of the ecosystem approaches to health into more traditional research methodology yields more accurate results.

Multidisciplinarity is the use of separate methodologies from different disciplines concurrently; transdisciplinarity, on the other hand, is a re-conceptualization of the research problems, objectives and methodologies in light of all relevant disciplines simultaneously (Nielsen 2001). Examining the health of individuals, households or populations in isolation yields an incomplete assessment; links across scales – to the village, region, national politics, ecosystem, etc. – are needed (Waltner-Toews and Kay 2005). This necessitates a transdisciplinary

approach that is in continual re-evaluation. Transdisciplinarity requires coordination and communication between traditionally isolated fields.

The first step of integrating gender and social equity analysis into ecosystem approaches to health research is deciding what to ask or what to look for (WHO 2002). If gender is a priority at the research planning stage, the questions that are asked may be different. In depth analysis of social justice and gender equality requires the collection of differentiated social variables, such as sex, caste, and ethnic group. Disaggregated analysis of social variables is essential to the ecosystem approaches to health in order to uncover potentially hidden trends in exposure or health status (Forget and Lebel 2001). Statistical approaches, such as stratification by sex, are important tools for analysing the differences between social groups and how gender interacts with other social and biological determinants of health. Care must be taken, however, when drawing conclusions, as sometimes it is not sex per se that determines an effect, but some factor related to sex. For example, in certain cases body size may be a better predictor of an outcome than sex (Sptzer 2010). Finally, the design of interventions must attempt to redress the inequalities that lead to differential exposure and risk if they are to be effective (Forget and Lebel 2001). In the Peruvian Amazon a recent study showed that women were more influenced by “ethnic beliefs” and would be more reticent to adopt solutions involving modern medicine than men, who have more contact with the outside world (Espinosa 2009); the author points out that taking into consideration the beliefs and hesitations of women is critical since they are the primary care givers in the community.

One of the first exercises that an EcoHealth research team undertakes is to identify all the stakeholders involved in the issue, including the researcher. Stakeholders from various interest groups are included in the identification of the problem and the design of the study. This approach not only ensures the pertinence of the research project but also builds confidence among participants (Forget and Lebel 2001). Nonetheless, participatory research is an ongoing

challenge for researchers in ecosystem approaches to health, both as a result of limited experience with the techniques and limited interest on the part of stakeholders. Forget (1997) has proposed an iterative research methodology whereby the determinants of health are identified first. The new knowledge garnered from the study of these determinants is then used to design interventions. Finally, the knowledge from all stages and stakeholders is used to develop indicators for measuring the effectiveness of the intervention. In this “action- research” approach each step is continually adjusted to the changing reality. The notion of risks and benefits can be useful in garnering support for research. Benefits can include better access to health care, increased knowledge, or socioeconomic incentives. Mertens et al. (2005) discuss using indicators of participants’ involvement in research activities to determine if there are barriers to participation by certain social groups. A more robust tool to determine if there are systemic barriers to participation is the use of social network analysis (Mertens et al. 2005). This approach allows researchers to identify individuals who participate less and determine if specific groups of people are being marginalized. Adapted participatory approaches can then be used to engage these individuals (Mertens et al. 2005).

2.1.4 An Ecosystem Approaches to Health Perspective Applied to the Current Study In the study presented in this dissertation, using ecosystem approaches to health implies taking into consideration the various causes of land-use change, multiple sources of contamination, compound exposure pathways, manifold stakeholders, and various health outcomes. Combining land-use research with the ecosystem approaches to health is a logical step, as both emphasize transdisciplinarity and holistic thinking. These approaches can be used to consider the broader implications of land-use change, mercury in local fisheries and petroleum exploitation on health outcomes. The situation is complex, as each environmental challenge exists alongside the other. Further, the forces behind these health outcomes act in synergy with other factors that affect health directly, such as

access to health care and education. Environmental changes expose populations to pathogens, inclement weather, toxic agents and natural disasters. People’s health status is influenced by these forces as well as their livelihood options. How peasants decide to make a living will in turn depend on the politico-economic, socio-cultural and biogeochemical forces at work in their communities, countries and regions.

In this section, several health outcomes of the current land-use patterns are outlined using the literature specific to the Andean Amazon. Then, some of the deleterious health outcomes of mercury contamination, one of the negative consequences of deforestation, are highlighted drawing on literature from indigenous populations around the world. The single most influential land-use change in the study area has been the exploration and extraction of crude oil. In the final section, some of the health consequences of petroleum exploitation highlighted in the literature on the study area are considered.

2.1.4.a Impacts of Land-Use Change on Local Communities The impacts of land-use change on local people span the social, economic and health realms. While many of these impacts have been identified, others likely remain unknown. The following sections document the impacts of land-use change that have been identified in the literature from the Andean Amazon.

Social impacts. The most extreme impact that land-use change can have on a people is their extermination. The Tetetes of the Ecuadorian Amazon were driven to extinction as oil companies took over their land in the 1970s (Little 2001). While less acute, also palpable in Andean Amazonia is widespread loss of traditional livelihoods, customs and beliefs. For some, this heralds an era of affluence, while others have difficulty adapting. For example, permanent settlement resulted in a decreased sense of perceived well-being among the Matsigenka of the Peruvian Amazon (Izquierdo 2005). Land-use changes can lead to unequal distribution of wealth, which Godoy et al. (2006b) correlates to feelings of anger and stress in foraging-farming communities of the Bolivian

Amazon. Finally, diverging interests and distrust have led to conflict and violence over forests (Jones 1995; Little 2001).

Nutrition. Changes in land use often translate into changes in resource availability or choice of cultivars, both of which can lead to malnutrition. Hodge and Dufour (1991) found growth retardation in a group of Shipibo from the Peruvian Amazon who were undergoing rapid acculturation and disruptions in their food supply. San Sebastian and Santi (1999) compared good nutrition among the Napura of the Ecuadorian Amazon to malnutrition in a neighbouring colonist village. They conjecture that the Napura’s commitment to their communal land provided them ample wildlife protein. Orr et al. (2001) found differences in nutritional status among two traditional Amerindian groups in the Andean Amazon to be related to resource availability. In contrast, Godoy et al. (2006a) found no secular trends in height as a group of Bolivian Amerindians integrated into the market economy, nor any impact of inequality on nutritional status (Godoy et al. 2005; Godoy et al. 2006b). A study among sedentary versus hunting-gathering Shuar in the Ecuadorian Amazon found that women of the acculturated, agricultural village had higher body fat and levels of insulin and leptin, biomarkers of diabetes and cardiovascular disease, than the more traditional groups (Lindgärde et al. 2004). Thapa et al. (1996) found that increased area in cultivation led to greater work for women. They comment on the potential impacts that increased farm labour could have on the health of the family, since women prepare meals and are usually the primary care givers.

Diseases. Land-use change has been credited with the emergence of diseases in the Andean Amazon. Malaria was considered eliminated from the Napo basin in the 1970s before large-scale clearing, but has since re-emerged (San Sebastian et al. 2000). Along the Iquitos-Nauta road, deforestation was found to promote the presence and biting rate of Anopheles darlingi, a common mosquito vector of malaria (Vittor et al. 2006; Vittor et al. 2009). In Loreto department of the Peruvian Amazon, the emergence of chloroquine-resistant Plasmodium

falciparum, another mosquito parasite, has been associated primarily with small pools on cleared land, fish farms, and areas of poor sanitation (Roshanravan et al. 2003). Transmission of leishmania in the Andean Amazon has been found to be highest around houses and close to coffee or cacao plantations (Richard Davies et al. 2000). Aguilar et al. (1999) have documented the emergence of endemic regions of Chagas disease in the Ecuadorian Amazon, while Patz et al. (2000) explain that the emergence of this disease is related to uncontrolled deforestation and colonization, which simultaneously eliminates wild hosts and places humans in contact with the species responsible for the disease: Trypanosoma cruzi. A similar mechanism could be behind the upsurge in hepatitis and an outbreak of rabies in the Peruvian Amazon both of which are associated with vampire bat bites (Augusto Lopez et al. 1992; Echevarria and Leon 2003). Finally, increasing conversion of land to urban areas is leading to concerns over epidemics of communicable diseases such as cholera (Schteingart and Saenz 1991; Tickner and Gouveia-Vigeant 2005).

Ecosystem services. The health and welfare of local people depend on the natural resource base and the ecosystem services that the local and global environments provide. de Koning et al. (1999) caution that continued agricultural expansion in the Ecuadorian Amazon will have serious impacts on soil fertility and biodiversity. Numerous studies have quantified the impacts of mechanized farming and pasture on erosion, soil compaction and decreasing soil macrofauna and fertility, thereby raising concern over the sustainability of such practices (Barber 1995; Woodward 1996; Moran et al. 2000; Decaens et al. 2004; Martinez and Zinck 2004; Mainville et al. 2006). Two studies in a national park along the Napo River, Ecuador, claim that biodiversity decreases as a consequence of petroleum company activities (Canaday and Rivadeneyra 2001; Bass et al. 2010). Kichwa in the region contend that hunting is getting progressively more difficult as petroleum development expands and that road construction across streams disrupts the migratory routes of fish (Kimerling 2001). Many fauna, like fish species that rely on flooded forests to feed, need large expanses of land in order to

survive. The worth of food, building materials, and medicines that local people once extracted from the forest can exceed the revenues from activities that have displaced forests (Laurance 1999) translating into more work and decreased leisure time (Behrens 1989, 1992). Land-use changes, specifically riverside agriculture and hydraulic gold mining, are having important impacts on water quality in the Andean Amazon leading to increased erosion and turbidity of rivers (Goulding et al. 2003; Mainville et al. 2006). Forest conversion could cause a substantial reduction in annual rainfall in the Amazon, where half of rainfall is a result of evapotranspiration (Salati and Vose 1984), with consequences for humidity, temperature, seasonality and, in some regions, the occurrence of wildfires (Laurance 1999). A recent study has documented an increase in forest fires in the Ecuadorian Amazon, a region where fires were thought to be impossible (Messina and Cochrane 2007). An entire body of literature is currently debating the contribution of the Amazonian forest and its destruction to climate change (Fearnside 1996; Laurance 1998; Fearnside 2001; Nepstad et al. 2009). Several studies have evaluated the global environmental services related to climate mitigation provided by western Amazonia (Naughton-Treves 2004; Saatchi et al. 2007).

Contamination. Contamination of the Andean Amazonian environment with persistent and toxic chemicals is a relatively new phenomenon. Well studied in the Brazilian Amazon, contamination of aquatic ecosystems and rural communities by mercury released through artisanal gold mining has been little studied in the Andean Amazon (Maurice-Bourgoin et al. 2000a; Ramirez Requelme et al. 2003; Counter et al. 2005). Mercury is a neurotoxic agent that negatively impacts development and neurobehavioral performance at exposure levels common in riparian communities of the Amazon (see Chapters 3, 4, and 5). Less work has been conducted on the mercury load of aquatic systems as a result of deforestation, despite the fact that 85% of the silt load to the Amazon River comes from this region (Loker 1996, p.54). A study by Mainville et al. (2006) associated deforestation and decreased mercury levels in soils, hypothesizing that

the missing mercury was leached to the river. A companion study related bioindicators of mercury exposure in rural communities to fish consumption (Webb et al. 2004).

A variety of studies in the Ecuadorian Amazon have linked petroleum extraction with incidence of cancer of the stomach, rectum, skin melanoma, soft tissue, kidney, cervix and lymph nodes (San Sebastian et al. 2001a; Hurtig and San Sebastian 2002a; Hurtig and San Sebastian 2002b; San Sebastian and Hurtig 2004; San Sebastian and Hurtig 2005). Other studies have associated exposure to hydrocarbons with spontaneous abortions (San Sebastian et al. 2002) and skin irritations (San Sebastian et al. 2001b). Increasing use of agricultural inputs, including pesticides and fertilisers, have negative impacts on human health. Hurtig et al. (2003) found that while users were aware of the risks, awareness raising should be a priority in the Ecuadorian Amazon where the most common pesticides are Paraquat and Glyphosphate. Prolonged or acute exposure to pesticides such as these can cause cancer, respiratory effects and skin disorders (Hurtig et al. 2003). Aerial fumigation of coca crops in the Colombian Amazon is a growing concern as winds carry the pesticides to neighbouring communities and dusters often miss their mark (Moreno-Sanchez et al. 2003). Finally, the release of sulphuric acid, ether, and acetone from the refining of coca into cocaine is a problem that grows proportionally with cocaine production (Jones 1995).

2.1.4.b Impacts of Mercury Contamination on Local Communities Mercury contamination in wild foods has direct and indirect consequences for indigenous populations. Since mercury is imperceptible in the environment and the consequences at doses typical in fish eating societies are subtle, this is often an “invisible” problem.

Toxic effects. The direct consequences of exposure to mercury are neurodevelopmental, neurobehavioral and cardiovascular (and are described in greater detail in Chapters 3, 4, and 5). Even slight disruptions in

neurodevelopment can have important consequences for the welfare of a generation (Wheatley and Paradis 1996; Hansen and Gilman 2005). Indigenous people who rely on fish have lifelong exposures that could have impacts different from the acute exposures seen in Minamata and Iraq that form the basis of our clinical knowledge (Dumont et al. 1998). More studies on the impacts of chronic, lower doses of mercury in indigenous populations are needed. Because nutrition and diet play a role in the metabolism and detoxification of methylmercury, modulating levels (Chapman and Chan 2000; Kuhnlein and Chan 2000; Passos et al. 2003), studies on impacts are needed for a wide variety of diets and exposure patterns. These studies are sorely lacking for indigenous groups in Amazonia.

Nutrition. If mercury levels are so high or the perceived risk so great that fish consumption is relinquished or curtailed, the impacts of mercury contamination change. The indirect consequences span health, economic and social aspects of life. As indigenous communities abandon traditional diets, food diversity decreases (Kuhnlein and Chan 2000) and intake of beneficial elements such as fatty acids diminish while saturated fat content increases. Diet transitions in indigenous communities are brought about primarily through contact with the industrialized society, but warnings about the fitness of wild foods or the perception of the quality of wild foods has played a role in some communities and for some people. Mercury contamination awareness among the Cree of Canada has been partly responsible for a general decrease in the consumption of fish (Belinsky et al. 1996). A move away from a traditional diet, and the reduction in physical activity that has accompanied it, has been associated with obesity, dental caries, anaemia, immune suppression and diabetes (Thouez et al. 1989), although current studies indicate that contaminant exposure likewise contributes to these diseases, notably diabetes and immune suppression (Dewailly et al. 2000; Van Oostdam et al. 2005b; Philibert et al. 2009).

Mental health. The consequences of this shift have also been felt in terms of mental health. Contamination of the environment is seen by most indigenous

people as a lack of respect and, therefore, can profoundly disrupt their sense of wellbeing. In addition, the value systems of many indigenous groups are predicated on the ability to provide for future generations. When this is compromised an individual’s sense of self-worth is at stake. Changes associated with less social and less active lifestyles have led to family and community violence, drug and alcohol abuse, and suicide. The collection of wild foods is an antidote to social problems as it endows the population with social cohesion, time outdoors, skills, and confirmation of their worldview (Kirmayer et al. 2000). In a final irony, traditional health systems, predicated as they often are on the consumption of certain foods that might be high in mercury (Borre 1994), are in jeopardy, leaving indigenous people with fewer customary ways to heal.

2.1.4.c Impacts of Petroleum Exploitation on Local Communities Contrary to mercury contamination, contamination by petroleum and land rights conflicts between communities and companies are conspicuous and influential.

Toxic and nutritional effects. Contamination of local ecosystems by petroleum leads to exposure to toxic chemicals, such as heavy metals, hydrocarbons and radioactive material brought to the surface through drilling (O'Rourke and Connolly 2003). In oil fields, along pipelines and in surrounding areas, polycyclic aromatic hydrocarbons (PAHs) – compounds composed of hydrogen and carbon and containing at least two benzene rings – are released into the environment though spills and the discharge of production waters (water that is drawn up with petroleum upon drilling). The deleterious impacts of PAHs on the physical health of populations are outlined in Chapter 6 and include, notably, cancer and adverse pregnancy outcomes. Whereas mercury contamination in fish is not visibly apparent at the levels found in the Andean Amazon, contamination by PAHs is often perceptible. Damage to fish includes conditions such as narcosis, mortality, decreased growth, edema, cardiac dysfunction, deformities, lesions and tumours of the skin and liver, cataracts, decreased immunity, estrogenic effects, and biochemical changes (Logan 2007). Many of the riparian populations in the

region depend on fish to meet their protein requirements and if they decrease their consumption of fish due to fear of contamination without access to a replacement many of the same health problems that have occurred as a result of mercury warnings could appear.

Ecosystem encroachment. Encroachment of petroleum activities into intact forests can decimate local populations of birds, mammals, and fish, making hunting and fishing more difficult for local people (Canaday and Rivadeneyra 2001; Finer et al. 2008). Road construction by oil companies has been partly responsible for disturbances to wildlife and also leads to high rates of deforestation. The equipment required to drill a well, including rigs, weighs millions of pounds, and the transportation and installation of this equipment can have negative impacts on the ecosystem (O'Rourke and Connolly 2003). The creation of bodies of standing water by oil companies can increase breeding grounds for the mosquito Anopheles sp., effectively increasing the incidence of malaria in the region (Martínez et al. 2007).

Conflict. The presence of the oil companies in the region is highly contentious (Sawyer 1997; Sabin 1998). Some people insist that the extraction of petroleum stop altogether, others support the economic activity and still others are asking for changes in how the industrial activity is carried out (Valdivia 2008). O’Rourke and Connolly (2003) have outlined four types of conflict that ensue from oil exploration and extraction: (a) territorial conflict; (b) civil unrest or war; (c) superpower geopolitics; and (d) terrorism targeting oil facilities. In Ecuador and Peru, conflict has primarily revolved around disagreements between indigenous people, the companies and the government over the use of indigenous territories, although several other levels of conflict have been witnessed (described below). I would argue that there is a fifth category of conflict: intra-community conflict fomented by the oil companies.

Protests and law suits against the companies and governments by local people have had as their primary goal to regain control of traditional territories and require companies to stop polluting ecosystems. Land titles are difficult to obtain for indigenous people and even if they are secured they do not include mineral or subsoil rights (Dussias 2007-2008). Protests over the extent of petroleum extraction, the negligent practices used by the companies and trespassing have erupted in many regions of the Amazon where oil exploitation is taking place (Sawyer 1997). The violent events of Bagua, Peru in June 2009, in which 32 people were killed, were the culmination of an attempt on the part of indigenous people to enter into negotiations with the government over two controversial bills that gave increased jurisdiction to foreign companies. Two class-action law suits are currently underway. The first is against Texaco, which operated in the northern Ecuadorian Amazon for decades leaving untold contamination in the region (Kimerling 2007). The second, in the Corrientes region of Peru, is against Occidental Petroleum and is also for environmental damages (Dussias 2007- 2008). These protests and law suits have created tension in the communities that are involved

The hostility that flared up between Peru and Ecuador in the 1990s over their mutual border running through the Amazon was not provoked by interest in natural resources such as petroleum, but this was one factor among others and some suggest that it will become a larger concern for both countries in coming years (Korzetz 1995). When protest against the construction of the Heavy Crude Pipeline was undertaken in the 2000s, war was threatened by the then president of Ecuador, Gustavo Noboa (Widener 2007). Several recent political developments in Peru have been influenced by the potential of petroleum revenue. Peru recently passed contentious bills aimed at encouraging foreign investment in the Amazon. The prospect of cheap non-Middle Eastern oil certainly weighed in Peru’s favour in the recent signing of free trade agreements with the United States and Canada. As of yet there has been little or no terrorist acts targeting oil facilities, since the

people opposed to oil extraction are primarily opposed to the contamination it causes.

Petroleum development has led to tension between partisans in some areas, such as the Pastaza region of Ecuador (Sawyer 2004) and the Corrientes region of Peru. This tension has been used by the companies to their own advantage following the old adage “divide and rule” (Sawyer 2004). In the case of both the Pastaza region of Ecuador (Sawyer 2004) and the Corrientes region (personal observation), oil companies have financed pro-business indigenous organizations to counter the locally formed indigenous groups whose main activity has been to protest the methods used by the oil companies in the region. The hostility in some communities is palpable and takes its toll on the well-being of individuals in small communities. Frustration has also arisen between allied indigenous groups and NGOs as a result of the stressful situation (Earle 2009).

Disempowerment. In intricate ways the development of the petroleum industry has disempowered local people and created distrust between local people and their government (Valdivia 2008). Peoples who were once sole decision makers in their own territory have had to come to terms with the reality of contested land rights within one generation. In most cases companies have established their operations in indigenous people’s territory with little or no consultation process, leading to feelings of helplessness and anger. Where consultation has taken place, federal agencies have required indigenous communities to choose one representative, in contradiction to their traditional methods of negotiation, which has led to situations of corruption (Gutierrez Choquevilca and Huboux 2006). Control over the reserves of oil determines who garners benefits from the sale of oil (O'Rourke and Connolly 2003). Privatization and mergers throughout the 1990s has led to a situation in which oil companies have harnessed the control of oil reserves retaining the vast majority of profits for themselves (O'Rourke and Connolly 2003). Valdivia (2008) argues that petroleum governance has historically marginalized people in Ecuador. Protestors’ attempts to repatriate their territory

and express their concerns have been viewed by the government as unpatriotic, furthering feelings of disempowerment. Studies have shown that the negative impacts of oil exploitation fall disproportionately on disadvantaged populations (O'Rourke and Connolly 2003). Sawyer (2002) has argued that some local people view the relationship in the terms of a “First-World man exploiting a Third-World woman.” Some who originally supported the petroleum companies have been disillusioned, realizing that the industrial activity did not bring with it the modernization of the region they had hoped it would (Valdivia 2008).

Boom towns and migrant workers. The presence of petroleum has led to the unregimented growth of urban centers in some areas (e.g. Coca, Ecuador) (Korzetz 1995). These towns often have no central square and lack essential services such as sewage treatment. All the health problems that are the hallmark of unsanitary urban conditions could be expected to erupt in these settings. An outbreak of cholera in the Peruvian Amazon in the 1990s affected urban citizens more than rural residents (Quick et al. 1996). Increased access to market goods has led to an increase in the use of alcohol, which has become a growing problem for women who suffer from domestic violence (Goicolea 2001). The arrival of migrant workers – almost exclusively men – has led to a demand for prostitutes, which brings with it the negative health outcomes – physical, mental and social – associated with this industry (Martínez et al. 2007). Further, the migrant workers occasionally bring with them diseases foreign to the local populations (Martínez et al. 2007). Many Urarina in the Peruvian Amazon have died as a result of measles and whooping cough imported to the region by oil workers (Witzig and Ascencios 1999). On the other hand, the urbanization of the Amazon has led to improved access to health care for some individuals.

2.2 Land-Use Change Research on land-use and land-cover change explores how humans change the ways in which they use land and how the biophysical aspects of the Earth’s surface change as a result (Meyer and Turner 1996; Skole 1996). Deforestation is

concentrated in “fronts,” or “hotspots,” several of which are located in the Andean Amazon (Myers 1993; Achard et al. 2002). Other regions of Amazonia are escaping deforestation pressure. Thus, the spatial patterns of land-cover change are heterogeneous and complex; yet, overall, the progression of humanized landscapes is alarming in its scale and pace. Since many of the environmental services that local populations depend on, such as the two studied in this dissertation – fisheries and water for household use – require intact ecosystems for their maintenance, an in depth study of the patterns and causes of environmental deterioration is necessary before embarking on research and interventions using the ecosystem approaches to health.

A widespread oversimplification is that growing population and poverty drive shifting cultivators’ land-use strategies (Heilig 1994; Lambin et al. 2001). However, a body of literature examining land-use decision making among populations is questioning the approach that restricts drivers of land conversion to the local level (Schelhas 1996; Pichon 1997b; Angelsen et al. 1999; Sunderlin et al. 2000). These case studies are pointing toward macro-level causes of land-use change, such as corporations, infrastructure, land tenure, international trade, input prices, foreign exchange and subsidies. Angelsen et al. (1999) divide the causes of land conversion into variables at three levels: direct sources (agricultural expansion, fuel wood collection, etc), immediate causes (output prices, wages, etc), and underlying causes (lead institutions, GDP, economic growth, debt, etc). Immediate causes are distinguished from underlying causes in that they enter into the land managers’ decision-making processes (Angelsen et al. 1999); whereas underlying causes reside in a larger playing field, yet influence the immediate causes. Thus, while forests might fall at the hand of the peasant, these peasants make decisions based on forces that are to a large extent ‘out of their hands.’

2.2.1 Land-cover Change in the Andean Amazon The Andean Amazon has among the highest rates of deforestation in the world. Myers (1993, p. 11) identifies two deforestation fronts in the Andean Amazon:

Western Amazonia, paralleling the Andes in Ecuador and Peru, and northern Bolivia, with annual deforestation rates of 3.0% and 2.6%, respectively. Achard et al. (2002, p.1001) estimate deforestation on the Ecuador-Colombia border to be progressing at 1.5%/year, while annual tropical forest clearing in the Peruvian Andes approaches 1%. Lambin et al. (2003) claim that deforestation is spreading from its epicentre in Brazil, just recently reaching the Andean Amazon. Innumerable land-cover change ‘silences’ also exist. Often these silences coincide with areas of social unrest, such as parts of Colombia and Peru (Sierra 2000; Walsh et al. 2003; Armenteras et al. 2006), or areas enjoying relative stability (Kaimowitz 1997).

In the Ecuadorian Amazon, land-cover change etches a fishbone pattern into forests following roads. Sierra (2000, p.5) estimates that in the Napo Deforestation front, cleared area doubled from 1986-1996, swathing 12.4% and impacting 16% of the region. He concludes that deforestation is proceeding at a rate of at least 1%/year, which is lower than earlier estimates (Myers 1993; Achard et al. 2002). Although deforested area increased, Mena et al. (2006) found that the rate of deforestation in the core colonization area decreased between the periods 1986-1996 and 1996-2002. Rudel et al. (2002) report significant reforestation in the southern region; however, they caution that it would be premature to deem this a forest transition. Fragmentation and patch edge increased throughout the Ecuadorian Amazon (Pan et al. 2004; Messina et al. 2006). Overall, the Ecuadorian Amazon constitutes a region of rapid land-cover change primarily following road patterns.

A dearth of information for the Peruvian Amazon make difficult the quantification of land-cover change over the past 30 years (Harcourt and Sayer 1996), but a recent study evaluated the deforestation rate in the Peruvian Amazon to be 645 ± 325 km2/year and noted that 86% of the damage was concentrated in two regions: Pucallpa and Puerto Maldonado (Oliveira et al. 2007, p.1233). The Smithsonian Atlas of the Amazon shows that deforestation is concentrated along roads in the

Andean foothills and along the Amazon River near Iquitos (Goulding et al. 2003). Early estimates of forest loss ranged between 9 and 16% (Garland 1995; Harcourt and Sayer 1996; Mäki et al. 2001). Along the interoceanic highway, modest net deforestation was observed between 1986-97 (0.1%/year) (Naughton-Treves 2004, p.179). Although data is missing for regions of Peru, the literature shows that significant areas of forest have been cleared in parts of the country.

2.2.2 Land-use Change in the Andean Amazon In contrast to the land-cover change studies reviewed above, which focus on regional analyses, numerous studies are available on land-use change conducted at the household level. I draw upon the most salient to illustrate the nature of land- use change in the region. Contemporary traditional livelihoods in western Amazonia generally combine subsistence and market-oriented agriculture with fishing, hunting, harvesting of non-forest timber products (NFTP), and/or timber collection (Loker 1993; Thiele 1995; Coomes and Burt 1997; Takasaki et al. 2001). ‘Andeanization’ has led to larger farms, pasture and the employment of technologies not adapted to the region (Garland 1995; Thiele 1995; Pichon 1997a).

2.2.2.a Agriculture. Most agriculture in Ecuadorian and Peruvian Amazonia is traditional swidden-fallow or market-adapted agroforestry (Padoch 1988b, a; Peck 1990; Coomes and Burt 1997). These practices create a patchy landscape, composed principally of forest interspersed with small fields (Pinedo-Vasquez et al. 2002)..

By 1991, peasants claimed over a third of the Ecuadorian Amazon (Southgate et al. 1991). Pasture represents up to 87% of land clearing (Wunder 1997, 5.3). Agricultural land tripled from 1974-1985 in Napo province (Eastwood and Pollard 1992, p.108). Household farms along roads or rivers are the main proximate cause of deforestation (Rudel and Horowitz 1993). Over half of households held cattle (Pichon 1997b) but larger, mature farms consecrated more

farm area to pasture (Pichon 1997a). Wunder and Sunderlin (2004) cite Latinos’ voracious appetite for beef as the main factor inhibiting the forest-protecting effect of oil exploitation in northern Ecuador. Coffee was once an important export crop in montane regions (Murphy et al. 1997), but infestations and unfavourable market prices have made this land use less lucrative (Eastwood and Pollard 1992; Marquette 1998). Small-scale cash cropping is still common (Pan et al. 2004); however, large-scale cattle operations and plantations are nearly absent (Eastwood and Pollard 1992). Settlement is primarily spontaneous, leading to unregimented land clearing (Rudel and Horowitz 1993).

In the Peruvian Amazon, swidden agriculture remains the dominant land use (Pinedo-Vasquez et al. 2002). Up to 80% of deforested land is dedicated to shifting cultivation (Escobal and Aldana 2003, p.1875), yet Garland (1995) estimates that only 20% of the cleared area is under cultivation due to the extensive nature of practices (p.219). Along the Amazon River near Iquitos, primary forest has been almost entirely replaced by secondary fallows and degraded pasture (Coomes et al. 2000; Mäki et al. 2001). Two studies found that half of farm land is in secondary vegetation (Smith et al. 1999; Coomes et al. 2000); yet, marked differences exist between households (Coomes et al. 2000). Pasture is the largest land-use category in the Pucallpa colonization front (Smith et al. 1999) and has been credited for land shortages on farms (Loker 1993). Coca production has proliferated since the 1970s (Pinedo-Vasquez et al. 1992) and pushes subsistence producers further into the forest (Garland 1995).

2.2.2.b Logging. Large differences in the nature and extent of logging exist in the Andean Amazon. Gullison et al. (1996) note a general absence of forests managed for sustained yield. In the Ecuadorian Amazon, there is no large-scale logging – concessions are banned (Southgate et al. 1991) – but settlers exert pressure on the forests (Messina et al. 2006). The few households that do participate in the timber trade (Pichon 1997a) cut only the most valuable species (Wunder 2005). Indigenous communities sell cutting rights to merchants (Pearman 1995) and

loggers work clandestinely, using petroleum company roads (Aguirre 2003). In the Peruvian Amazon, lumbering is primarily selective (Bodmer et al. 1988) and dominated by companies with multiple, small contracts centred in Pucallpa and Loreto (Smith et al. 2006). Studies have found that charcoal production is not an important cause of deforestation, as it is integrated in swidden-fallow agroforestry (Coomes and Burt 2001; Labarta et al. 2008). The literature indicates that household use constitutes the major logging pressure in Ecuador while commercial logging compounds household use in Peru. A study carried out in Ecuador and Bolivia suggests that certified wood is still too marginal of a commodity to have much impact on conservation in tropical countries (Ebeling and Yasué 2009).

2.2.2.c Non-Timber Forest Products (NTFP). Early accounts heralded NTFP as a solution to deforestation (Peters et al. 1989; Grimes et al. 1994). More recently the sustainability of NTFP extraction has been called into question (Stagegaard et al. 2002; Coomes 2004). A study of forest use in north-eastern Peru has shown that almost every product destined for markets was collected to extinction (the exception being rubber) and that no species attribute (e.g., high reproduction rates) could ensure sustainability (Coomes 1995). Indirect environmental impacts from extractivist land use further threaten forests, as harvesters supplement their incomes through agriculture, timber harvesting, and livestock (Escobal and Aldana 2003). Generalizing about trends in NTFP use is difficult as reliance on these products is heterogeneous (Takasaki et al. 2001; Coomes 2004; Coomes et al. 2004); however, Gavin and Anderson (2007) hypothesize that communities with more indigenous people and longer residence time will concentrate more on forest extraction. Ultimately, the sustainability of NTFP harvesting depends on good management, though fluctuations in market prices and migration make sustainable resource management difficult (Coomes 1995).

2.2.2.d Mining. Gold and oil are the most heavily mined commodities in the Andean Amazon. Small-scale gold mining is prevalent in the Madre de Dios

region of Peru where mechanized gold mines have razed vast areas (Goulding et al. 2003). The Ecuadorian and Peruvian Amazon have been occupied by oil companies since the 1960s (Little 2001; Armenteras et al. 2006), and fossil fuel exports are the foundation of their regional economies (Wunder and Sunderlin 2004; Etter et al. 2006b). The Ecuadorian Amazon has been almost entirely subdivided into oil concession blocks (Little 2001); yet, deforestation for oil operations is negligible in comparison to the extent of land clearing executed by colonists who have settled in the more than 10,000 km2 opened by the 500 km oil- road network (Kimerling 1990, p.849). Further, state oil revenues have been channelled into colonization schemes (Wunder 2005) and additional road construction, facilitating frontier migration (Wunder and Sunderlin 2004). Wunder and Sunderlin (2004) conclude that the Dutch disease effect, whereby exports of oil supplant agriculture, curbed deforestation in the Ecuadorian Amazon in the 1970s, but, since, forest conversion to agricultural land has accelerated.

2.2.2.e Conservation, Ecotourism and Environmental Services. Amid widespread deforestation, there exists a nascent network of protected areas, although, governments’ lack of commitment to conservation has been criticized (Kimerling 1990; Eastwood and Pollard 1992; de Koning et al. 1999; Sierra et al. 2002). Yasuní National Park is the only strictly protected area in Ecuador (other areas allow oil prospection) (Bass et al. 2010). In Peru, only 12% of the Amazon is protected against oil extraction (other protected area statuses allow extraction) (Finer et al. 2008, p.e2932). Messina et al. (2006) explain how downgrading, to permit small-scale agriculture and logging, has reduced pressure in and around the Cuyabeno reserve, Ecuador. Several authors suggest an approach targeting the local people most dependent on forest resources when constructing conservation strategies (Coomes et al. 2004; Gavin and Anderson 2007).

Ecotourism can provide local people an incentive to restrict deforestation and combat land-use change by external agents, as was the case when the tourism

sector lobbied successfully for the doubling of the Cuyabeno Reserve and obtained a decree prohibiting oil activities (Wunder 2000). Further, ecotourism can limit the amount of time people have to invest in clearing land, hunting and fishing (Wunder 2000). Finally, a study of an indigenously owned ecotourism lodge in the Peruvian Amazon suggests that locally owned enterprises are one way of avoiding people-park conflicts (Ohl-Schacherer et al. 2008). On the other hand, research in Peru indicates that increased revenue from paid work in the tourism sector, leads to the ability to intensify hunting and fishing expeditions and farming efforts (Espinosa 1998; Stronza 2007). Payment for environmental services, such as averted green house gas emissions, is a new incentive used to regulate land use allocation.

In summary, agricultural expansion is the primary proximate cause of deforestation in the Andean Amazon. Pasture is the single most expansive land use in Ecuador and Peru, where household farming dominates. Timber companies are active in Peru, while household timber needs are placing pressure on forests in all regions. There is no consensus on the role of NTFPs in forest change, yet recent studies suggest that extraction is being practiced unsustainably. Gold mining has led to significant land damage in Peru, while the oil industry, through building roads, has facilitated the colonization of vast areas of Ecuador. Finally, conservation and ecotourism provide some hope that not all of the Andean Amazon will be converted to field and pasture.

2.2.3 Drivers of Land-use Change A burgeoning body of literature has examined the drivers of land-use change in Ecuador and Peru. Deforestation is a result of proximate causes and underlying driving forces that work in concert. The drivers of land-use change are complex and place specific. Mena et al. (2006) have found that drivers at the farm level are different from drivers at the community level. Temporal differences complicate the situation. Time lags create difficulties in correlating land-use changes and socio-economic drivers (Behrens et al. 1994). Finally, multiple drivers can have a

synergistic effect. The drivers of land-use change can be categorized into the politico-economic factors that influence deforestation including poverty, roads and market integration, land tenure, market prices, and government policies; the socio-cultural variables that play a role in determining the direction and extent of deforestation: traditional practices, population growth and out-migration; and, finally, the biogeochemical characteristics of the region that have been implicated as the cause of rapid forest conversion, namely soil fertility (or lack thereof).

2.2.3.a Population Growth. The number of migrant farmers in the Andean Amazon is among the highest in world (Myers 1993; Brown and Sierra 1994). Laurance (1999) has shown that two-thirds of the variation in forest conversion between the different Amazonian countries can be explained by the number of people residing there. He concludes that population growth is the main cause of deforestation, with other factors playing a secondary role. Almost all authors agree that the influx of people settling along oil company roads is a main driver of deforestation in the Ecuadorian Amazon (Rudel and Horowitz 1993; Murphy et al. 1997; Pichon 1997a; Marquette 1998; Pan et al. 2004; Pan et al. 2007). Second generation migrants have been found to stay in the Ecuadorian Amazon, often migrating to other rural areas, exerting pressure on intact ecosystems (Barbieri et al. 2009). Pichon (1997a) found that availability of in-house labour was the single most influential household attribute for deforestation. However, in a distant region of southern Ecuador, Sirén (2007) found the rate of deforestation for subsidence agriculture by indigenous people to be low considering high population growth. In the Peruvian Amazon, deforestation slowed from 1991–97 despite continued population growth (Naughton-Treves 2004) and Garland (1995) contends that labour scarcity prompts deforestation, since weeding takes more labour than clearing new forest.

Although net in-migration has been a major factor accelerating forest conversion throughout the Andean Amazon, authors disagree on its relative importance and a debate is crystallizing over the underlying drivers of migration. In summary, both

push and pull factors are at work: migration is driven by poverty and landlessness, and directed by environmental heterogeneity, lead institutions, growth coalitions, public policy and access to markets.

2.2.3.b Poverty. Most authors agree that land shortages in the Andes have played a key role in the destruction of rainforests (Eastwood and Pollard 1992; Rudel and Horowitz 1993; Brown and Sierra 1994; Garland 1995; Painter 1995; Pichon 1996; Etter et al. 2006a). However, there is disagreement over the role of poverty. Poverty alleviation was found to have no impact on forest loss in the Ecuadorian Amazon (Wunder 2001). Growing revenues for the Ecuadorian middle-class, associated with oil exports, led to increased demand for beef, thus stimulating frontier deforestation (Wunder and Sunderlin 2004). Similarly, Zwane (2007) suggests that small income increases among the poor in Peru does not reduce land clearing, especially in households where labour is not a limiting factor. Some people are in fact too poor to put much pressure on the forest ecosystem because they lack assets and savings (Rudel and Horowitz 1993; Coomes and Burt 2001). In brief, it appears that poverty drives certain patterns of land use, such as migrant, peasant agriculture and extensive farming, while affluence is implicated in other patterns, namely export cash crops and pasture.

2.2.3.c Roads and Market Integration. Where roads exist they have almost invariably led to rapacious deforestation by settlers. But some claim that roads are simply a ‘locational determinant’ of deforestation (Mäki et al. 2001). Gavin and Anderson (2007) posit that integration into local markets is one of the most important factors determining forest resource use. Road construction, financed by oil companies, has been pivotal in the deforestation process of the Ecuadorian Amazon. Pichon (1997a) found that farms closer to roads had greater percentages of their land cleared and in perennial crops and pasture. Within 20 years of the announcement of the construction of a road leading into the Andes, colonists in the Chiguaza River Basin had cleared half of the land (Rudel and Horowitz 1993). Finally, market integration has a similar influence on indigenous communities as

it does on mestizo communities in the Ecuadorian Amazon (Gray et al. 2008). In contrast, Walsh et al. (2008) claim that in recent years, land closer to roads and communities have been converted to secondary forest as people find off-farm employment.

Eighty-three percent of Peru’s total deforestation was found within 20km of the nearest road (Oliveira et al. 2007, p.1235). The construction of the interoceanic highway, aimed at alleviating landlessness in the highlands, led to a roadside annual deforestation rate of 1.1% (Naughton-Treves 2004, p.181). A time series analysis of deforestation between Iquitos and Nauta (100km upriver) found that deforestation showed peaks in years of road extension (Mäki et al. 2001). Peralta and Kainer (2008) found that distance from market alone was not sufficient to determine market integration in Asháninka communities of southern Peru: families needed access to labour to divert efforts from subsidence to market activities. In south-western Amazonia, roads are often built by unofficial interest groups and lead to highly fragmented forest mosaics (Perz et al. 2008). In summary, forests penetrated by roads almost invariably experience pressure by settlers. The pattern of road building in the Andean Amazon is irregular, concentrated in the Andean foothills and criss-crosses a large expanse of the Ecuadorian Amazon.

2.2.3.d Out-migration. While migration to the frontier regions has had a strong impact on land-use change, out-migration is also occurring in certain localities. Two contending theories explain the impacts of urbanization and industrialization on rural land use: the ‘hollow frontier theory’ stipulates that as people seek better opportunities in urban areas, cattle ranchers or mechanized farmers buy up and consolidate abandoned land. As a result, forest is often lost. In the ‘forest transition’ theory, sub-standard and remote land reverts to forest as settlers re- establish themselves in cities (Rudel et al. 2002). Rudel et al. (2002) observed a potential forest transition in Southern Ecuador; however, in the north, Pichon (1997b) found that settlers commuted between city and rural homes, creating a

hollow frontier without consolidation where labour-conserving cattle ranching dominated. Another study has found that urban migration is more important among women than men (Barbieri and Carr 2005), which would support the hollow frontier scenario in which men remain to run cattle farms. Population density in the Muyuy floodplain, Peru, is among the highest in the Amazon, but population growth is not deemed a major concern due to out-migration (Pinedo- Vasquez et al. 2002). Migrants to cities influence land-use patterns through their role as consumers: the increasing demand for building materials for the recently established urban poor in northern Peru has led to a decrease in agricultural land and an increase in secondary forest (Padoch et al. 2008). Urbanization and out- migration have been under-studied in the Andean Amazon (Barbieri and Carr 2005) and, consequently, no consensus exists on their role in land-use change.

2.2.3.e Soil Fertility. In models referred to as the ‘peasant pioneer cycle’ (Pichon 1997b), the ‘barbecho crisis’ model (Maxwell 1980) or the ‘malaise of the minifundio’ (Foweraker 1981), continued deforestation is conceived of as a method of escaping the straightjacket of poor Amazonian soils. The applicability of this conceptual framework to the Andean Amazon, where soil fertility is better than in the Brazilian Amazon, is being called into question (Thiele 1993; Pichon 1997b). In a study in the Ecuadorian Amazon, few people complained of low soil fertility owing to volcanic deposits, yet deforestation rates were high (Pichon 1997b). Recent reappraisals of swidden-farming suggest that labour requirements and yields do not differ significantly on fallowed land versus primary forest (Thiele 1993). Two studies, one in Colombia and the other in Ecuador, found that high soil fertility was one of the best predictors of deforestation (Marquette 1998; Etter et al. 2006a).

2.2.3.f Land Tenure. Insecure land tenure incites people to deforest for two reasons. First, insecurity prevents households from engaging in perennial cropping or sustainable practices requiring more labour (Pinedo-Vasquez et al. 2002). Second, informal and formal land laws have generally recognized a

household’s tenure to land through their use of it (Perreault 2003). In the Ecuadorian Amazon, many authors contend that land security is a major contributor to deforestation (Rudel 1983; Southgate et al. 1991; Pichon 1997b; Perreault 2003). On the other hand, Pichon (1997a) argues that those people without land tenure control less land and therefore even if they clear high percentages of their land, their contribution to overall deforestation is less than large-land holders with secure land tenure. Still in Ecuador, Rudel (1995) found that in small, colonist communities, informal societal controls exist that acknowledge property rights and discourage encroachment, leading to little forest clearing. In the Peruvian Amazon, 61% of rural households are squatters and deforest twice as much as neighbours with land titles (Garland 1995, p.228). Land ownership-by-use occurs at a national scale as well: 10 of 14 colonization projects studied by Rudel (1989) were along the Rio De Janeiro line separating Peru and Ecuador in a futile attempt by the Ecuadorian government to lay claim to the region (p.439). While there is some disagreement, it appears that improving land tenure could reduce deforestation in some parts of the Andean Amazon.

2.2.3.g Market Prices. As market integration becomes more important for local livelihoods, commodity prices have been found to influence deforestation rates (Southgate et al. 1991; Pinedo-Vasquez et al. 2002). Rudel and Horowitz (1993) note that the rates of deforestation in the southern region of the Ecuadorian Amazon paralleled prices of agricultural commodities more than population increases. In the Loreto district of the Peruvian Amazon, Espinosa (2008) found that volatile and primarily low market prices for staple agricultural goods have steered people away from agriculture and increasingly toward extraction of wildlife and forest products. Ultimately, the profitability of increasing an area under cultivation is determined by the relative price that the crop will fetch to the cost of labour (Thiele 1993).

2.2.3.h Governments. Some observers claim that, in the end, forest conversion is a result of a lack of government resolve to curb deforestation or bad policy

choices (Jones 1995). In the last 30 years almost all Andean countries experienced agrarian reforms premised on the values and practices of the mestizo culture and requiring substantial portions of landholdings to be cleared to prove ownership (Perreault 2003). In the 1980s, the Ecuadorian and Peruvian governments hoped to turn the Amazon into a ‘bread-basket’ (Myers 1993). An era of government subsidies, followed by development aid, has been responsible for its share of deforestation, mostly for cattle ranching and cash cropping (Rudel and Horowitz 1993; Thiele 1995; Coomes 1996; Pinedo-Vasquez et al. 2002; Alvarez and Naughton-Treves 2003; Perreault 2003; Naughton-Treves 2004; Arce-Nazario 2007). The cessation of credit to small farmers in Peru has been recognized as the cause for an increase in abandoned fallow since 2005 in an area south of Iquitos (Arce-Nazario 2007). On the other hand, some analysts have claimed that structural adjustment programmes have spawned poverty and a search for new land among the impoverished (Perreault 2003; Pacheco 2006) or promoted conversion of forest for export crops (Steininger et al. 2001). Others note diminished deforestation corresponding to fiscal austerity (Naughton-Treves 2004). Finally, a lack of clarity in laws has allowed logging companies to engage in irresponsible practices in the Peruvian Amazon, yet the strict laws in the Bolivian Amazon have been deemed a success (Smith et al. 2006).

A myriad of other forces have been put forth as drivers of deforestation, including: infrastructure, such as schools and electricity (Behrens et al. 1994; Pan et al. 2004); technology, such as chainsaws (Kaimowitz 1997; Pichon 1997b); land speculation (Rudel and Horowitz 1993; Mäki et al. 2001); natural catastrophes, such as severe flooding and drought (Behrens 1989; Pacheco 2006); higher education and a desire to increase standard of living (Pichon 1997b); household lifecycle (Pan et al. 2004) and external debt (Gullison and Losos 1993; Myers 1993). The drivers of land-use change in the Andean Amazon are inherently complex and place-specific, making generalizations difficult and, perhaps, inappropriate.

2.3 Conclusion Through the use of holistic approaches such as the ecosystem approaches to health we can enhance our understanding of the health impacts of environmental changes. Before embarking on research to evaluate the impacts of land-use change, the nature of land-use change must be adequately understood. Elucidating the causes of land-use change is a challenge but it is particularly crucial for planning impact assessments, models, and projections for ecosystems, and in designing interventions in the communities reliant on the environmental services provided by an intact ecosystem. Often immediate drivers of land-use change are local features, such as topography, soil fertility, and land tenure, while the underlying drivers, such as export markets and geopolitics, play out at national and global scales, as well as the local scale. The review of the literature on land- use change in Ecuador and Peru has highlighted important differences in the land- use change patterns between the two: (1) small-scale agriculture is the primary direct cause of deforestation in Ecuador, whereas in Peru a combination of small- scale farming and large-scale enterprises (coca and logging) are responsible; and (2) the presence of oil roads in Ecuador has led to extensive deforestation, whereas, an absence of roads in Northern Peru has left large areas untouched. The review of the literature on impacts has highlighted several key areas in which the current land-use change pattern in the Andean Amazon is negatively impacting local people’s health: contamination, decreased nutrition, conflict, new diseases, violence, etc. This in-depth analysis of the context, in conjunction with the results presented in the following chapters, can help inform interventions and policy recommendations.

Chapter 3: Comparison of Mercury in Ichtyofauna along Three Rivers of the Andean Amazon (Ecuador and Peru)

3.1 Introduction Food security and nutrition are linked to productive and healthy fisheries in many regions of the developing world (Tontisirin et al. 2002). This is the case in the Amazon where fish provide a free, high quality source of protein, energy and micronutrients, unparalleled by many crops advocated in food security strategies (Wahlqvist 2005.). Epidemiological studies highlight the role of fish consumption in disease prevention and mental health (Vanschoonbeek et al. 2003; Fung et al. 2004; He et al. 2004; Timonen et al. 2004; Whalley et al. 2004; Whelton et al. 2004; Leaf 2008). However, epidemiological studies have also demonstrated a link between fish consumption and mercury (Hg) levels in the Amazon (Boischio et al. 1995; Lebel et al. 1997a; Boischio and Henshel 2000a; Dolbec et al. 2001; Webb et al. 2004). Studies have shown that levels lower than originally thought cause measurable neurological harm in both adults and children (Lebel et al. 1996; Lebel et al. 1998b; Dolbec et al. 2000; Cordier et al. 2002; Mergler 2002; Yokoo et al. 2003). Other compications include cardiovascular toxicity (Fillion et al. 2006) and immunotoxicity (Silbergeld et al. 2005). New WHO recommendations set the maximum weekly intake to 1.6 µg per kg body weight per week of mercury (FAO/WHO 2006). Mercury appears to be jeopardizing one of the Amazon’s most productive food sources.

Sources of Mercury in the Amazon. The Andes is one of the main mercuriferous belts on earth (Nriagu and Becker 2003) and soils originating from volcanic ash are rich in mercury (Hernandez et al. 2004; Mainville et al. 2006). Soil erosion, provoked by deforestation, leads to the leaching of naturally- occurring mercury into aquatic environments (Roulet et al. 1999; Fostier et al. 2000; Roulet et al. 2000; Mainville et al. 2006). The present study was carried out

in the world’s largest, ancient humid tropical alluvial fan, the Pastaza Megafan (Räsänen et al. 1992), composed of volcanically derived alluvial and where, in addition to anthropogenic erosion, current tectonic movements cause heightened soil erosion (Laraque et al. 2004; Bès de Berc et al. 2005).

Petroleum extraction is another potential source of mercury and other heavy metals, such as lead and cadmium (Bloom 2000a; Wilhelm 2001; Martínez et al. 2007; Wilhelm et al. 2007). Crude oil from South America has on average 5.3 µg/kg of Hg, higher than in Africa (2.7 μg/kg), the Middle East (0.8 μg/kg), the United States (4.3 μg/kg) and Canada (2.1 μg/kg) (Wilhelm et al. 2007). The practices used by companies in the region (dumping of production waters into rivers and streams and the burning of unwanted gases), in addition to spills, introduce the mercury found in crude oil into the environment (Martínez et al. 2007). Atmospheric deposition of mercury from the burning of fossil fuels is a major source of mercury (NRC 2000) and the practice of burning gas that escapes when petroleum is drilled would be expected to release Hg into the atmosphere. Mirlean et al. (2005) found Hg concentrations in the precipitation of an industrial area of Brazil to be seven times the South American average and attribute this to the presence of a local petroleum refinery.

Artisanal gold mining, not present in the study region but common in parts of the Brazilian Amazon and the southern parts of the Peruvian Amazon, involves the use of metallic mercury, and high mercury concentrations are found in fish in the vicinity (Palheta and Taylor 1995; Malm 1998; Maurice-Bourgoin et al. 2000a; Mol et al. 2001; Durrieu et al. 2005). Another well studied source of mercury is hydroelectric dams, where mercury from flooded soils enters the aquatic ecosystem and where high levels of organic matter enhance the bacterial activity responsible for mercury methylation (Reuther 1994; Kehrig and Malm 1999; Boudou et al. 2005).

Whereas many studies on mercury levels in fish have been carried out in the Brazilian Amazon, only a few have focused on the Upper Amazon (Maurice- Bourgoin et al. 2000a; Webb et al. 2004), despite the fact that the Upper Amazon is an area of intense deforestation and active petroleum extraction. The present study is the first to present Hg levels in the ichtyofauna of three rivers of the Upper Amazon with contrasting deforestation and natural resource development patterns: the Corrientes River in Peru (low deforestation and high petroleum activity); the Napo River in Ecuador (heavy deforestation and petroleum activity); and, the Pastaza River in Peru (intermediary deforestation upstream from the study area and petroleum activity in the upper reaches of the study area). These rivers are all unaffected by contamination from other human-made sources of mercury, namely gold mining and hydroelectric production.

Sources of mercury are not spread uniformly throughout the Amazon and the levels of methylmercury (MeHg) – the form of mercury that moves easily through the food chain – are not distributed equally in ichtyofauna. Spatial differences tend to be less important than interspecific differences (Lewis and Chancy 2008), meaning that fish from the same species sampled in different regions tend to have similar concentrations if no point sources significantly increase mercury levels in the environment. Mercury levels in fish are positively correlated with both the size and age of fish (Grieb 1990; Berninger and Pennanen 1995; Driscoll et al. 1995) and piscivorous fish (fish that eat primarily other fish) are known to have higher concentrations than herbivorous fish (fish that eat primarily plants and fruits) due to the bioaccumulation and biomagnification of mercury in the aquatic food chain (da Silva Brabo et al. 2000; Maurice-Bourgoin et al. 2000a; Webb et al. 2004; Sampaio da Silva et al. 2005). Predatory fish are, therefore, more responsive to differences in environmental mercury levels because they biomagnify the mercury in their environment, concentrating it up to 106 times (Baudo et al. 1990).

Some Amazonian fish species, notably catfishes, are known to migrate long distances (hundreds of kilometres), feeding in a variety of habitats (Barthem et al. 1991; Barthem and Goulding 1997) and, therefore, can accumulate mercury from several localities. For this reason, non-migratory fish are used as indicators of water quality (Belger and Forsberg 2006). Piscivorous, non-migratory fish species can be used to determine the mercury load in specific areas of a river system, to compare with other regions and to elucidate the influence of environmental conditions on mercury levels. Hoplias malabaricus (fasaco in Peru and guanchiche in Ecuador), which is associated with floating meadows in lagoons (Correa et al. 2008), has been found to be an accurate indicator species (Belger and Forsberg 2006).

The aim of this study was to determine mercury levels in the ichtyofauna of three rivers with contrasting land-use characteristics in the Andean Amazon, compare the levels with those in other studies, and to explore the differences among the three rivers using Hoplias malabaricus as an indicator species.

3.2 Methods Study area. Fish were collected in common fishing sites along three rivers in the Andean Amazon (also known as the Upper or Western Amazon): the Corrientes River, Peru; the Napo River, Ecuador; and the Pastaza River, Peru (see Figure 1.1). The three rivers are biogeochemically similar, all being neutral to alkaline, white water rivers with unpredictable polymodal flood pulses resulting from rainfall in the headwater region of the Andes. Creeks and lagoons in the region are black water and the three rivers drain Andean volcanic soils. There are no marked wet and dry seasons and the annual rainfall is 2-4m/year. The diversity of fish in the Upper Amazon is remarkable. There are approximately 562 species in the Napo River Basin (Galacatos et al. 2004, p.37); over 800 documented in the Peruvian Amazon, with estimates that place the species count as high as 1200; and 312 recorded species in the Pastaza River (Ortega and Hidalgo 2008, p.261).

In addition to the routine practices and numerous spills that have taken place over the years in the study area, a spill resulting from the collapse of a section of a pipeline passing through Peruanito, on the Corrientes River, occurred four and a half months prior to sampling (Aste Daffos 2006). It is not known how many barrels of crude oil were released but the spill covered an area of 7,820 square metres (92 m * 85 m) and the extent of the direct damage is estimated to be 11,800 m2 (Aste Daffos 2006, p.3). However, because rains can carry the crude oil into adjacent micro watersheds, the area impacted by the spill is estimated to be much larger than this (Aste Daffos 2006).

Sampling. We asked fishers in nine villages (Corrientes: Peruanito, Copal, Nuevo Paraiso; Napo: Palma Roja, San Carlos, Añangu, Pañacocha; and Pastaza: Loboyacu, Alianza Capahuari) and one town (Coca) along the three rivers (see Figure 3.1) for a small sample of their catch. Sampling of fish was not random, but attempted to represent as many consumed fish species as possible, as recommended by Burger et al. (2006). Fish were identified, measured and weighed. Up to 10g of flesh was cut from the tail muscle. Specimens of Hoplias malabaricus were caught in seven locations (Corrientes: Negra Lagoon, Piuri Lagoon; Napo: Añangu Lagoon, Piguali Lagoon, a pond near Pañacocha; and Pastaza: the Pastaza River near Loboyacu and Capahuari Lagoon). Samples were placed in Nalgene™ scintillation vials and frozen until analysis. No sampling permits were required by the Ecuadorian or Peruvian governments for this sampling strategy, nor was ethics approval from the ethics review board at McGill University required. In all, 486 fish were sampled during three visits to the region (2001 and 2003, see Webb et al. (2004); and 2006). Information on the feeding regime of the fish – piscivore, carnivore (fish that eat primarily insects and crustaceans), omnivore, benthivore (fish that eat bottom-dwelling organisms), detritivore (fish that eat detritus) and herbivore – were collected from fishers and the scientific literature.

Mercury analysis. Analysis of total mercury in the fish samples was performed at the Geochemistry and Geodynamics Research Centre (GEOTOP) laboratory, UQAM-McGill, using cold vapour atomic fluorescence spectrometry (CVAFS) following a modification of the method developed by Bloom and Fitzgerald (1988). The technique is described in greater detail in Pichet et al. (1999): after an acid digestion, total mercury is reduced to elemental mercury in the presence of

SnCl2. It is then vaporized and transported by argon into an atomic fluorescence spectrophotometer, where mercury levels are measured. The detection limit was 0.002 μg/g. Analytical quality was ensured by including samples of powdered fish (tort-2 from the National Research Council of Canada, Institute for National Measurement Standards, Calibration Services, Ottawa, Canada), as well as two acid blanks in series of 30 samples.

Statistics. All statistics were carried out using the programme JumpIn 5.0.1a. A multiple mean comparison using Tukey’s HSD was performed to examine differences between trophic guilds. A regression model was built to best describe the mercury concentration in Hoplias malabaricus as a function of selected predictors known to influence mercury concentrations (weight of the fish and location). Multiple mean comparisons using Tukey’s HSD were used to describe differences between Hoplias malabaricus in two lagoons along the Napo River. Statistically significant results at p-values of ≤ 0.01, ≤ 0.05 and ≤ 0.1 are given.

3.3 Results

3.3.1 Descriptive Statistics As expected, we found high fish species diversity among our samples: 61 species were identified among the 486 specimens; many species were rare, but six species (Crenicichla sp, Mylossoma duriventre, Prochilodus nigricans, Serrasalmus rhombeus, and Hoplias malabaricus) accounted for 50% of the catch. Mylossoma duriventre (palometa) and Prochilodus nigricans (bocachico), two smaller fish low on the food chain, made up 29% of the catch. Piscivores and carnivores

together comprised 48%, 49% and 35% of the catch in the Corrientes, Napo and Pastaza rivers, respectively. Table 3.1 summarizes the weight and mercury levels of 30 of the 61 species, classified by trophic guild, and in the three river basins separately (range = 0.002-3.0 μg/g, wet weight). Species for which there were fewer than five specimens were not included in the table with the exception of certain piscivores with high Hg concentrations. Several large fish (Brachyplatystoma spp.) contained very high levels of mercury (up to 3.0 μg/g, wet weight). Table 3.2 presents the percentage of total fish, carnivorous fish and piscivorous fish exceeding the WHO safety recommendation of 0.5 μg/g, wet weight for each of the rivers and overall. Fifteen percent of piscivores were found to have levels above the recommendations. Other categories of fish had no samples exceeding the WHO safety recommendations.

3.3.2 Mercury Concentrations in Trophic Guilds A logarithmic transformation was performed on mercury concentrations to normalize the data. A multiple mean comparison using Tukey’s HSD was then performed to compare among six trophic guilds. Figure 3.2 shows the distribution of mercury levels in the six food regimes for 480 fish samples. As expected, piscivores are seen to have the highest levels (n = 141, μ = 0.28 μg/g, SD = 0.33) and the herbivores the lowest (n = 152, μ = 0.04 μg/g, SD = 0.03). The Tukey test showed four significantly different categories. Piscivores (D) had significantly more mercury than all other categories. Carnivores (C) contained significantly more mercury than the detritivores and the herbivores, whereas the herbivores (A) had significantly less mercury than all food regimes except the detritivores.

Table 3.1: Mercury concentrations (μg/g, wet weight) in 30 fish species (422 fish) collected from the Corrientes (C), Napo (N) and Pastaza (P) regions. Continued

Trophic Guild Common Name Mean weight (g) Mean Hg (μg/g, wet weight) ±SE (n) Latin name Peru/Ecuador Rivers: C, N, P Corrientes Napo Pastaza Herbivores Mylossoma duriventre* Palometa 92, 265, 385 0.025±0.007 (8) 0.017±0.006 (11) 0.034±0.006 (20) Prochilodus nigricans* Boquichico/ bocachico 311, 425, 525 0.066±0.009 (13) 0.05±0.003 (88) 0.0358±0.013 (3) Rhytiodus microlepis* Lisa negra 415, -, 583 0.01 (1) - 0.039±0.014 (4) Detritivores Curimata sp* Ratacara/ lloron 60, 155, 79 0.065±0.018 (5) 0.053 (1) 0.061±0.007 (10) Psectrogaster sp* Chio-chio 163, -, 64 0.064±0.013 (2) - 0.053±0.016 (8) Pterygoplichthys multiradiatus* Carachama/ raspa -, 298, 119 - 0.014±0.008 (3) 0.016±0.003 (4) Benthivores Chaetobranchus flavescens Bujurqui 93, -, 99 0.055±0.019 (3) - 0.089±0.012 (8) Omnivores Brycon melanopterus* Sabalo cola negra/ sabalo -, 1130, 445 - 0.068±0.02 (5) 0.09±0.05 (3) Leporinus friderici* Lisa 72, 307, 696 0.074±0.023 (3) 0.051±0.017 (7) 0.044±0.005 (8) Tetragonopterus chalceus Mojara/ojona 34, 65, - 0.1±0.022 (8) 0.015 (1) - Triportheus angulatus* Sardina 60, -, 51 0.101 (1) - 0.211±0.047 (6) Carnivores Crenicichla sp* Anashua/ vieja 40, 44, - 0.111±0.006 (5) 0.045±0.006 (18) - Pimelodus blochii* Cunchi/ barbudo 68, 52, 83 0.118±0.059 (2) 0.06±0.014 (5) 0.148±0.02 (11) Serrasalmus rhombeus* Pana blanca 50, 365, 20 0.06 (1) 0.204±0.038 (20) 0.046 (1) Serrasalmus spilopleura* Pana negra 900, 420, 320 0.906 (1) 0.649 (1) 0.464 (1) Piscivores Arapaima gigas* Paiche Not available - 0.44 (1) - Brachyplatystoma filamentosum Zungaro salton/ bagre sapote 33000 - 0.71±0.20 (13) - Brachyplatystoma flavicans Zungaro dorado/ bagre plateado 8375 - 0.54±0.17 (2) - Brachyplatystoma vaillanti Manitoa 905, -, 800 1.26 (1) - 0.17±0.14 (2) Cichla monoculus* Tucunare 620 0.14±0.025 (5) - - Cynopotamus amazonus Denton 68, -, 52 0.25±0.1 (3) - 0.301±0.101 (3) Hoplias malabaricus* Fasaco/ guanchiche 568, 501, 280 0.15±0.026 (11) 0.16±0.016 (14) 0.17±0.024 (10) Hydrolycus scomberoides* Huapeta 77 - - 0.443 (1) Pimelodella sp* Bagre 69 0.11±0.008 (2) - -

Pinirampus pirinampu Mota 760, 2238, 1302 0.54 (1) 0.22±0.04 (4) 0.078±0.02 (3) Pseudoplatystoma fasciatum Doncella/ bagre rayado 2203 - - 0.45±0.18 (3) Pseudoplatystoma tigrinum Tigre zungaro/ bagre pintadillo 3050 - 0.65 (1) - Pygocentrus nattereri* Pana roja 137 - 0.109±0.023 (24) - Rhaphiodon vulpinus* Chambira/ pez perro 515, 279 - 0.629±0.107 (7) 0.47±0.12 (5) Salminus hilarii* Sabalo macho 110 0.184±0.009 (8) - -

Notes: * Indicates resident species

Table 3.2: Percentage of sampled fish exceeding the WHO safety recommendation (0.5 μg/g, wet weight) by river and by trophic guild.

Corrientes Napo River Pastaza Overall River % (n) % (n) River % (n) % (n) Carnivores 8 (12) 8 (50) 7 (14) 8 (76) Piscivores 8 (38) 23 (71) 13 (32) 15 (141) Total 5 (105) 8 (245) 4 (131) 6 (486)

Figure 3.2: Box plot displaying Hg concentrations (μg/g, wet weight) on a log scale according to feeding regime. The groupings created using Tukey’s HSD are indicated on the x-axis. Cross hatches represent the maximum and minimum. Horizontal line represents the grand mean.

3.3.3 Mercury Concentrations in Hoplias malabaricus The length of Hoplias malabaricus specimens ranged from 15 to 47 cm (n = 35, μ = 33.9 cm, SE = 5.9) and weight varied from 115 to 950 g (n = 35, μ = 459.1 g, SE = 189) (see Table 3.1). Total Hg (wet weight) varied from 0.073 to 0.374 μg/g (n = 35, μ = 0.16 μg/g, SD = 0.073). Hg was regressed on length and weight separately for Hoplias malabaricus to assess which gave a better fit. The intercept was forced through zero. Mercury was similarly related to length (r2 = 0.84) and weight (r2 = 0.83). The slope was significantly different from zero (P < 0.0001) for both lines. Since the relationships were not distinct, weight was chosen over length for further analysis as this has been used previously for this species (Belger and Forsberg 2006; Dorea et al. 2006). As the distribution of weight was not normal, weight was log transformed.

The pattern of Hg accumulation in Hoplias malabaricus in the three regions was examined using a regression model. The model including log weight, region and the interaction of region and log weight as model effects and log Hg as the dependant variable showed the best fit for Hoplias malabaricus (P = 0.0003) (see Table 3.3). The Q-Q plots from the GLM indicate a good fit and the ANOVA was robust. There was no significant lack of fit error (P = 0.51). The three parameters – region, log weight, and the interaction of region and log weight – were all significant (P = 0.0016, P < 0.0001, and P = 0.02, respectively). The dummy variable for the Corrientes region was significantly different from the Pastaza region, whereas the Napo region was not significantly different from the Pastaza. Similarly, only the interaction term including the Corrientes Region was statistically different. These parameters explain 58% of the variation in Hg concentration. The significance of the interaction term – region x log weight – shows that the regression on the covariates has a distinct slope for the Corrientes region. This indicates a difference in Hg concentrations in the Corrientes region that is independent of the differences in the weight of the fish sampled there and that the rate of increase in Hg with respect to weight is also different.

Table 3.3: Regression model of log mercury concentrations in Hoplias malabaricus, wet weight (μg/g), Andean Amazon.

Covariate Coefficient (t ratio) Constant -8.36 (7.32) Log weight 1.04 (5.63) *** Region dummy R1 (Corrientes) -0.44 (3.79)*** Region dummy R2 (Napo) 0.03 (0.29) Interaction log weight x Region dummy 0.75 (2.53)** R1 Interaction log weight x Region dummy -0.15 (0.59) R2 R2 0.58 F 6.59 P(F) 0.0003 Number of observations 35

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01

The linear regression of log mercury concentrations in Hoplias malabaricus versus log weight shown separately by river demonstrates that there are important differences in the rate of Hg accumulation between the three rivers (see Figure 3.3). The slope of the line is highest in the Corrientes region; intermediate in the Napo region and lowest in the Pastaza region (see Table 3.4). As the weight of the fish increases, the mercury concentration rises fastest in the Corrientes region, followed by the Napo and, finally, the Pastaza. The significance of the interaction term in the regression model shown in Table 3.3 confirms that the slope of the line for the Corrientes is significantly different from the Napo region and the Pastaza region.

3.3.4 Mercury Concentrations in Hoplias malabaricus on the Napo River On the Napo River, a significant difference was found between the mercury concentration in Hoplias malabaricus in two of the lagoons (Mann Whitney, P=0.02). Hoplias malabaricus from Laguna Piguali, Pañacocha (μ=0.2 μg/g, n=7) had higher Hg concentrations than Hoplias malabaricus from Añangucocha, Añangu (μ=0.12 μg/g, n=6) (see Figure 3.4). This difference is present despite the fact that there was no significant difference in the weight of Hoplias malabaricus from the two lagoons: Pañacocha (μ=511 g, n=7) and Añangu (μ=493 g, n=6) (Mann Whitney, P=0.25) (see Figure 3.5). This difference is also shown in the graph displaying Hg concentrations vs. weight (see Figure 3.6). The disparate slopes of the lines for the two villages are shown on the graph and in Table 3.5. The distribution of both Hg and weight was normal in the Hoplias malabaricus of the Napo region.

Figure 3.3: Hg concentration (μg/g, wet weight) vs. weight (g) on log scales for Hoplias malabaricus in the three regions (Corrientes (°),Napo (+), Pastaza (x)).

Table 3.4: Regression equations and R2 for log Hg concentration (μg/g, wet weight) in Hoplias malabaricus from three regions of the Andean Amazon.

Region Equation R2 No. of fish Corrientes River -13.33 + 1.79 log weight 0.934 11 Napo River -7.4 + 0.89 log weight 0.387 14 Pastaza River -4.35 + 0.45 log weight 0.217 10

Figure 3.4: Hg concentration (μg/g, wet weight) of Hoplias malabaricus in two villages of the Napo region. Horizontal line represents the grand mean.

Figure 3.5: Weight (g) of Hoplias malabaricus in two villages of the Napo region. Horizontal line represents the grand mean.

Figure 3.6: Hg concentration (μg/g, wet weight) vs. weight (g) of Hoplias malabaricus in two villages of the Napo region (Añangu (+) and Pañacocha (x)).

Table 3.5: Regression equations and R2 for Hg concentration (μg/g, wet weight) in Hoplias malabaricus from two communities on the Napo River, Ecuador.

Region Equation R2 No. of fish Añangu 0.03 + 0.0001 weight 0.83 6 Pañacocha 0.02 + 0.0003 weight 0.217 7

3.4 Discussion Mercury levels in some top-level predators in the study region – resident and migratory – are above WHO recommendations. This finding can form the basis for making diet recommendations in two regions where no prior studies have been published on Hg concentrations. The evidence further shows that the rate of increase in Hg concentration in Hoplias malabaricus according to the body weight of the fish is highest in a recently contaminated lagoon along the Corrientes River. This finding indicates that Hg is bioaccumulating at a faster rate in this heavily polluted area than in the other two regions, one of which has been deforested to a large extent, suggesting that inputs of petroleum and drilling wastes contribute to the Hg load of the ecosystem.

Mercury levels in certain resident species, especially piscivores, are above the WHO recommendations and migrant species bring Hg into both the local ecosystem and the diet of residents. The highest value in a resident species, Rhaphiodon vulpinus (chambira/pez perro), was double the recommended maximum level of 0.5 μg/g. Levels in one large catfish were six times the recommended concentration. The levels found here are generally lower than those reported in the literature for Amazonia, but the specimens sampled also tended to be smaller. Appendix 2 summarizes the Hg levels in resident, predatory fish species from the literature.

Many studies reported in the literature have focused on sites heavily contaminated through gold mining: the Madeira River (Malm et al. 1989; Pfeiffer et al. 1989b; Pfeiffer et al. 1991; Kehrig and Malm 1999; Boischio and Henshel 2000b; Bastos et al. 2006; Kehrig et al. 2008), the Tartarugalzinho River (Bidone et al. 1997a), the Mutum Parana River (Reuther 1994), the Beni River (Maurice-Bourgoin et al. 1999; Maurice-Bourgoin et al. 2000a), Cachoeira do Piria (Palheta and Taylor 1995; Lima et al. 2005), Alta Floresta (Hacon et al. 1997a), Amapá State (Guimaraes et al. 1999) and sites in Suriname (Mol et al. 2001) and French Guiana (Richard et al. 2000). Bento Gomes River, in the Panatanal, Brazil, is the

only gold mining region that showed lower Hg levels than those found in our study (Lacerda et al. 1991). The authors offer a possible reason for such low levels in a region draining tailings from gold mining: the water flow is extremely high, effectively diluting the amount of Hg in the ecosystem. Studies from the mid and lower Tapajós River show high levels of Hg (Bidone et al. 1997b; Lebel et al. 1997b; Castilhos et al. 1998; da Silva Brabo et al. 2000; de Souza Lima et al. 2000; Santos et al. 2000; Uryu et al. 2001; Kehrig et al. 2008). This area of the Tapajós River is contaminated primarily due to the leaching of naturally occurring Hg in the soils following deforestation (Roulet et al. 1999; Roulet et al. 2000).

Other studies assess Hg levels in recently constructed reservoirs (Reuther 1994; Porvari 1995; Kehrig and Malm 1999; Kehrig et al. 2008) or where river chemistry favours the methylation and bioaccumulation of Hg (Guimaraes et al. 1999; Belger and Forsberg 2006; Dorea et al. 2006; Kehrig et al. 2008). The Negro River, a black water river, has a high concentration of podzols in the drainage basin resulting in high levels of dissolved organic carbon (DOC) (Kehrig and Malm 1999). High levels of DOC create opportunities for Hg to transport through the ecosystem (Kehrig and Malm 1999). Both black and clear waters, such as those in Suriname and French Guiana, have a low pH, which augments binding of Hg to particulate matter and increases methylation through favouring the oxidation of Hg0 to Hg2+ (Lacerda and Salomons 1998).

Lower Hg levels were to be expected in the region studied here because there is no history of gold mining or reservoir construction on these rivers; rather, volcanism, deforestation and pollution from the oil industry contribute to Hg loads. Further, since these rivers flow from the piedmont region of the Andes, where the slope of the terrain is more accentuated than in central Amazonia, the water flow rate is higher than in the majority of rivers reported on in the literature and Hg levels are possibly diluted. Fast moving waters provide fewer methylation sites, and fish living in rocky habitats with fast flowing water tend to be smaller,

as evidenced by the smaller size of most of the fish caught for this study as compared to other studies.

Whereas Hg levels in resident species tended to be lower than elsewhere, migratory species caught in the study area had high levels. Fish migration can serve as a dispersal agent for Hg accumulated elsewhere (Kehrig and Malm 1999). Indeed, the Hg levels in some of the large migratory piscivores, for example Brachyplatystoma spp., Pinirampus pirinampu, and Pseudoplatystoma spp., caught in the study region, are similar or higher than those reported on the Tapajós River (Bidone et al. 1997b; Lebel et al. 1997b; Castilhos et al. 1998; da Silva Brabo et al. 2000; de Souza Lima et al. 2000; Uryu et al. 2001), the Madeira River (Malm et al. 1989; Boischio and Henshel 2000b), the Jamari River (Reuther 1994), in Alta Floresta (Hacon et al. 1997a) and on the Beni River (Maurice- Bourgoin et al. 1999). Our samples of migratory fish were lower in Hg than those reported in Itaituba, Brazil (Santos et al. 2000), the Madeira River and tributaries (Pfeiffer et al. 1991), French Guiana (Richard et al. 2000), and the Beni River, Bolivia (Maurice-Bourgoin et al. 2000a).

As expected, piscivores and carnivores display higher concentrations of Hg than other trophic guilds in all three river systems. The type of fishing that was carried out in the three regions explains the observed differences in the percentage of piscivores and carnivores that exceed WHO recommendations for Hg content. Along the Napo River some samples were taken at the market in Coca where the urban population makes it profitable for fishermen to catch extremely large fish. In the Pastaza and the Corrientes basins, there is not a sufficient population density to support this type of fishing. Further, there is no refrigeration to conserve excess fish meat. Consequently, the percentage of fish exceeding the 0.5 μg/g limit is higher in the Napo region. If the fish sold at the Coca market are excluded from the analysis, the percentages exceeding the WHO health limit in the Napo basin approach those found in the other two regions: 6% of all fish, 8% of carnivores, and 15% of piscivores. Whereas the high proportion of herbivorous

fish observed in this study represents what some rural populations eat, it does not necessarily reflect what urban populations are exposed to. As seen in the Coca market, piscivores are overrepresented. In Coca, this might not be a problem since previous studies have shown that this population does not rely heavily on local fish for protein (Webb et al. 2004); however, in Iquitos, in the Peruvian Amazon, fish is a staple and in other cities of the Peruvian Amazon migratory, piscivorous fish represent over 90% of the landings (Ortega and Hidalgo 2008, p.262). On the other hand, the proportion of the catch made up of catfishes is likely to decrease due to overfishing (Ortega and Hidalgo 2008).

This study uncovered differences in the pattern of Hg bioaccumulation in Hoplias malabaricus, a resident piscivore, in three biogeochemically similar regions. Mercury levels in fish are known to be influenced by environmental conditions such as pH, DOC, conductivity and the types of soils in the drainage basin (Belger and Forsberg 2006). These factors do not differ significantly between these three rivers: all are basic, have high levels of DOC, similar conductivity and drain volcanically derived soils. So what else might explain the important differences we observed between the rates of bioaccumulation of Hg in the Corrientes, Napo and Pastaza watersheds?

The regression model of Hg in Hoplias malabaricus showed that in addition to the weight of the fish, region explains the observed Hg levels. Mercury was found to increase at a higher rate with respect to the weight of the fish in the Corrientes region. This was unexpected because the riparian forests of the Corrientes River are relatively intact, whereas the extent of deforestation in the Napo River basin is vast. If deforestation were the only explanation of Hg levels in these regions we would expect to see a gradient of Hg levels according to the deforestation rates in the three basins. An elevated rate of deforestation in the Napo River basin would be anticipated to lead to greater leaching of soil and higher Hg levels in Hopilas malabaricus. The Pastaza River, with deforestation upstream, would be expected to have the second highest levels of Hg bioaccumulation in Hoplias malabaricus.

The Corrientes, with minimal deforestation, would then have the least Hg bioaccumulation. But this is not the case: the highest rate of Hg increase was found in the Corrientes region, followed by the Napo and finally the Pastaza.

Inputs from the petroleum industry are a plausible explanation for the pattern we have observed. All but two of the samples on the Corrientes River came from Negra Lagoon, a lagoon connected to an area where a spill had occurred four and a half months prior to our sampling and where inputs of petroleum such as this have been occurring for the last 35 years. Similarly, Mirlean et al. (2005) found that the slope of the relationship between Hg concentration and the size of the fish in an industrial area of southern Brazil was greater than in a protected area.

Another possible explanation for the difference is the type and quantity of river transport and oil exploration detonation activities. Vessel wakes can cause riverbed erosion, although the extent to which this occurs is not known. The Corrientes River and the Napo River are frequently traveled by boats, primarily boat traffic associated with the activities of the petroleum companies, whereas the Pastaza River is less frequently visited. It has also been suggested that the detonation activities associated with seismic testing can lead to erosion (Hurtig and San Sebastian 2002a). Although exact figures are not available, there is more flooded forest in the Peruvian study sites. This could possibly explain the higher Hg content in Hoplias malabaricus from the Corrientes sampling sites as compared to the Napo sampling sites, but not the difference found between the Pastaza sampling sites and the Corrientes sampling sites.

Our results also showed a difference in the Hg levels in Hoplias malabaricus between two of the lagoons along the Napo River. A possible explanation is the presence of petroleum companies in Pañacocha. When the samples were taken, large scale drilling had not yet begun, but companies had been prospecting in the Pañacocha region since 1982. Another factor that might explain these results is the fact that the Añangu lagoon is located in Yasuní National Park, where no

deforestation is permitted. The residents of Añangu have disallowed the use of outboard motors in this lagoon to safeguard the wildlife. Laguna Piguali, where the samples from Pañacocha were caught, was in a protected area until it was taken over in 1982 for prospection. Fourteen oil wells in the Pañacocha oil field go into production in the second quarter of 2009 and are expected to produce 25,000 barrels of oil per day. It is not known yet whether a road will be constructed to the Pañacocha oil field; however, if this were to be the case we would expect the road to engender the same magnitude of deforestation seen further to the west where roads have been built.

3.5 Implications The results of this study implicate petroleum activities in contributing to the Hg load of aquatic ecosystems in the Andean Amazon. Fish from a recently contaminated lagoon bioaccumulated more Hg than fish from lesser or uncontaminated areas. Further, deforestation, another important source of Hg, is linked to road construction. In the Napo River basin roads are opened by petroleum companies (Pichon 1997a). Given that the Pastaza Megafan is highly susceptible to erosion (Guyot et al. 2007) and that these volcanic soils have a high Hg load (Mainville et al. 2006), forest conservation strategies should be a high priority in this region. The Yasuní National Park, located on the southern banks of the Napo River, is protected, but until the new Ecuadorian constitution was adopted in 2008, oil exploration was ongoing (Finer et al. 2008). Initiatives such as the Napo Wildlife Center, a community owned and operated ecolodge, located on the Añangu lagoon, are an effective way of supporting conservation. National parks exist on the Ecuadorian side of the Pastaza River but there are none on the Peruvian side, despite the fact that the entire Achuar territory in the Pastaza and Corrientes basin has been designated a Ramsar Wetland, the Abanico del río Pastaza (la Torre Lopez and Napolitano 2007). No parks exist or are planned in the Corrientes River Basin. Suitable tracts of forests should be identified and pressure put on the government to create protected areas in these watersheds. Any protected area that is created should exclude all possibility of petroleum

extraction, since our research and other studies show that Hg levels are higher in fish from industrial areas than in protected areas (Mirlean et al. 2005).

Since local people eat not only resident fish species, it is important to consider the Hg concentrations in all species. Several species of resident fish present levels of Hg higher than WHO recommendations, and migrant species, which tend to have very high levels of Hg, especially the catfish, are a source of contamination in the diet of local people. Because of the importance of fish in the diet of local people and no anticipated cessation of Hg inputs, there is reason for concern. The WHO safety limit, 0.5 μg/g, is based on 400g of fish per week. Local people eat up to seven fish meals a week (see Chapter 4), each portion being roughly 250g. The consequences of this sort of chronic exposure are just now being discovered (for a review see Passos and Mergler 2009). Finally, Hg has toxic effects on the fish themselves (Mela et al. 2007; Filipak Neto et al. 2008) and the impacts that this might have on fish health and stocks have not been fully explored, but our current research indicates that local people are observing changes (see Chapter 4). In order to safeguard the health of riparian populations in the Amazon it is important to have region specific advisories on Hg levels in fish species.

A more detailed study of the effects of petroleum extraction is needed to determine the amount of Hg in production waters, emanating from open flares, released during spills and in precipitation. Studies on the types of chemicals used by petroleum companies, especially emulsifiers, which contain heavy metals (O'Rourke and Connolly 2003), should be conducted. Laws exist that require companies to reinject production waters and cease using open flares. Companies are also required to carry out Environmental Impact Assessments, yet private firms are hired by the companies, a system lacking transparency (Finer et al. 2008). Independent verification that companies are complying with the laws is necessary in order to reduce the amount of heavy metals and other contaminants released to the environment.

Chapter 4: Methylmercury in Hair of Riverine Populations along Three Rivers in the Andean Amazon (Ecuador and Peru)

4.1 Introduction In many parts of the world people rely on wild foods for a significant portion of their diet. For populations living near rivers and lakes in Amazonia, fish provide an excellent source of protein, vitamins and minerals. Recently, though, high levels of mercury have been found in the aquatic food chains of the Andean Amazon (Maurice-Bourgoin et al. 1999; Maurice-Bourgoin et al. 2000a; Webb et al. 2004). At issue is whether local people should continue eating their traditional foods and risk the consequences of mercury toxicity on health, or alter their livelihoods and diet, potentially enduring nutritional, socioeconomic, and cultural disruptions. Ideally, local people would have access to information on mercury levels in fish and the factors that influence mercury absorption and toxicity in order to adjust their diet toward fish with lower mercury concentrations and foods that can moderate mercury absorption and toxicity; but, this information is lacking for many regions of Amazonia.

Studies have identified artisanal gold mining, where mercury is used to bind gold from rock, soils, or sediments, as one of the major sources of mercury in South America (Pfeiffer et al. 1993; Counter et al. 2005). Hydroelectric dams also have been shown to increase the bioavailability of mercury (Kehrig and Malm 1999). In addition, the Andes is one of earth’s main mercuriferous belts (Nriagu and Becker 2003) and soils originating from volcanic ash have high mercury concentrations (Hernandez et al. 2004; Mainville et al. 2006). Deforestation has been posited as the source of high mercury levels in some regions (Fostier et al. 2000; Roulet et al. 2000; Mainville et al. 2006). As soils are leached, mercury is transported to neighbouring aquatic environments. Petroleum extraction is another anthropogenic source of mercury to local aquatic ecosystems due to the mercury content in crude oil (Bloom 2000a; Wilhelm and Bloom 2000), substandard

practices used for extraction in the region (Martínez et al. 2007) and its role in creating one of the most active deforestation fronts in the world, the Napo deforestation front (Webb 2005).

Aquatic food chains in Amazonia are complex (Goulding et al. 1996) and conditions are favourable for the methylation of mercury (Pfeiffer et al. 1989a; Guimarães et al. 2000a; Guimarães et al. 2000b; Mauro et al. 2001). Methylation increases the uptake of mercury in the gastrointestinal tract (Gochfeld 2003). Concentrations for piscivorous fish often exceed 0.5 μg/g (Maurice-Bourgoin et al. 1999; Maurice-Bourgoin et al. 2000a; Webb et al. 2004), the limit for safe consumption (based on a diet containing 400g of fish per week) (WHO 1990). Fish consumption is considered the main vehicle of mercury exposure among riparian populations of the Amazon (for a review see Passos and Mergler 2009). World Health Organization (WHO) recommendations set the maximum weekly intake to 1.6 µg per kg body weight per week of mercury (FAO/WHO 2006) and large-scale longitudinal studies have been used to assess that mercury intakes from 0.1 to 0.23 µg/kg/day do not pose appreciable risk (for a review see Mergler et al. 2007), but these values have been questioned (Stern 2005a). In the Brazilian Amazon, a study calculated high daily mercury intakes, with 86% of participants surpassing 0.1 µg/kg/day (Passos et al. 2008, p.83). On the other hand, a traditional lifestyle, including daily fishing and frequent fish consumption, was found to be positively associated with an individual’s perception of quality of life, particularly among younger people (Fillion et al. 2009). Other studies have examined the influence of diet on mercury absorption and toxicity. Passos et al. (2007a) found that frequent fruit consumption modulates mercury exposure, with those who eat more fruits presenting lower bioindicators of mercury for the same amount of fish consumption. Lemire et al. (2006) found elevated selenium levels in the Brazilian Amazon and a more recent study showed a beneficial influence on mercury induced, age-related cataracts (Lemire et al. forthcoming).

The nervous system is the principal target of methylmercury (Clarkson 1987) (for a review see Castoldi et al. 2001). The first impacts of high level exposure, such as those that occurred in Minamata and Iraq (Gochfeld 2003) are non-specific: paresthesia (abnormal sensations), discomfort, and blurred vision (WHO 1990). At higher doses patients suffer from constriction in the visual field, ataxia (lack of muscular co-ordination), hearing impairment, dysarthria (impairment of speech), and tremors. In extreme cases, a coma or death can occur (WHO 1990). Small neurons in the central nervous system are especially susceptible because they have limited repair capabilities (WHO 1990). Methylmercury easily passes the placental membrane and accumulates on the foetal side (Clarkson 1993), making the foetus is more vulnerable to lower exposure levels (Chang et al. 1980) (for a review see Castoldi et al. 2004).

Recent studies in the Amazon and Andean foothills have documented neurobehavioral changes at mercury concentrations much lower than the value officially associated with clinical signs of methylmercury poisoning (>50 μg/g) (WHO 1990) in both adults (Lebel et al. 1996; Lebel et al. 1998a; Dolbec et al. 2000; Mergler 2002; Yokoo et al. 2003) and children (Counter et al. 1998; Crump et al. 1998; Grandjean et al. 1999; Cordier et al. 2002; Counter et al. 2002; Counter 2003; Chevrier et al. 2009) (for a review see Passos and Mergler 2009). Several longitudinal studies have assessed the neurodevelopmental impacts of chronic exposure to lower doses of methylmercury in children of fish eating populations. In the Faroe Islands, prenatal mercury exposure was negatively correlated with success on cognitive and motor tests at both seven and 14 years of age (Grandjean et al. 1997; Debes et al. 2006) and the data suggests that some damage is irreversible (Murata et al. 2004). Studies in New Zealand also found that neurobehavioral setbacks were associated with mercury exposure (Crump et al. 1998). Yet, in the Seychelles Islands cohort, early tests indicated no negative impacts, but tests at 9 years old showed that fine motor skills were compromised (Myers et al. 2003; Myers et al. 2009).

Whereas the primary effects of methylmercury are localized in the central nervous system, other impacts are being uncovered. Mercury interferes with protein synthesis (WHO 1990) and enzymes are inhibited by the disruption of sulfhydryl groups (NRC 2000). Amorim et al. (2000) suggest that methylmercury interferes with spindle function and chromosome segregation, and Silva-Pereira et al. (2005) found that low doses may be cytotoxic/genotoxic. Methylmercury seems to negatively affect the immune system and especially the developing immune system (NRC 2000; Silbergeld et al. 2005). Organic mercury can accumulate in the heart, leading to hypertension and an abnormal heart rate (NRC 2000). Acute myocardial infarction (MI) and coronary heart disease have also been linked to mercury in the diet (Guallar et al. 2002; Yoshizawa et al. 2002; Stern 2005b). Higher mercury levels have also been associated with higher blood pressure (Fillion et al. 2006; Valera et al. 2009).

The aim of this epidemiological study is to report on the levels of mercury in the hair of indigenous, riverine populations along three rivers of the Andean Amazon, a region little studied to date, and to make comparisons among the three rivers and eight communities. The ecosystem approach to health framework is used to contextualize the findings.

4.2 Methods Study area. The present study was carried out along three white-water rivers in the Andean Amazon (also known as the Upper or Western Amazon): the Napo River, Ecuador; the Pastaza River, Peru; and the Corrientes River, Peru (see Figure 1.1). Although there are no marked wet and dry seasons, December to February is somewhat drier and May and June are somewhat wetter. The annual rainfall is 2-4 metres. There is no gold mining or hydroelectric dams in any of the three basins, however, each river displays a different land-use pattern: the Corrientes River has low deforestation and high petroleum activity; the Napo River is experiencing heavy deforestation and petroleum activity; and, the Pastaza

River exhibits intermediary deforestation upstream from the study area and petroleum activity in the upper reaches of the study area.

Populations and recruitment. The study was carried out with people in eight villages along the three rivers (Napo River: Palma Roja, San Carlos, Añangu; Corrientes River: Peruanito, Copal, Nuevo Paraiso, and Pastaza River: Alianza Capahuari and Loboyacu) (see Figure 1.1). The populations are primarily indigenous peoples of the Kichwa, Achuar and Urarina nations. Most people practice agriculture, fishing and hunting; some people do work occasionally for the oil companies and/or the tourism industry. All villages have primary school; while in most villages secondary education is attained through visiting teachers. Health services and visits to a dentist are difficult to access due to the cost and distance. In all but one of the villages (San Carlos) the nearest city is only accessible by boat.

At each village the study was explained in a general meeting to all residents in attendance. Permission to conduct the research in the community was obtained from the community leader and the community members collectively at this meeting. After the communal meeting, each individual in the community was visited separately and invited to participate on a voluntary basis. All adults were eligible and no one incurred reprisal for not participating. No compensation was provided. Ethics approval was obtained from the McGill University Ethics Review Board. No ethics approval from the Ecuadorian or Peruvian government was required.

Based on mercury levels in similar communities, the necessary sample size was calculated to be approximately 200 individuals. Two hundred and twelve people 15 years and older were invited to join the study. Fourteen people refused. In total, 198 people (93%) were interviewed. Of these, 192 (97%) consented to give a hair sample. Interviews and sampling took place in a private space in the

informant’s home. The informed consent form was read aloud and participants signed. The villages were visited between July and December, 2006.

The community of Añangu was visited on a previous trip (2002) in the context of another study. The same methodology was used and a nearly identical questionnaire was administered to participants. In 2002, hair samples and questionnaires were collected from 24 individuals, 10 of whom also contributed in 2006. Construction of an ecolodge, The Napo Wildlife Center, in the community had just begun in 2002 and was completed in 2003. The 2002 data was compared with the 2006 data to determine if changes in mercury concentrations had occurred over the period 2002-2006.

Questionnaires. The questionnaire (see Appendix 1) was validated for cultural context in a previous study in the region (Webb et al. 2004). The questionnaire consisted of approximately 35 short questions organized into five sections – personal information (age, sex, ethnic group), health (smoking, drinking, health problems), occupation, fishing, and diet (including water). The questionnaire took approximately a half an hour to complete. Diet questions focused on the frequency (number of times per week), species and provenance (location of fishing) of fish consumed. Three questions to respondents addressed changes in fish quality and quantity: Have you noticed any changes in the fish in recent years? In comparison with 10 years ago, is the fishing better, worse or the same? In your opinion, why is this? In comparison with 10 years ago, do you eat more, less or the same amount of fish? Why is this? Ten years was chosen as a reference point to capture long-term trends in diet.

Estimate of mercury intake. Three hundred and eleven samples of fish were collected in the communities visited. The results of the mercury in fish analysis are presented in Chapter 3. The mercury concentrations in these fish samples were used as the Hg concentration in the most commonly eaten fish species each individual reported in the questionnaire. The mean of these Hg concentrations was

then calculated. Spatial differences tend to be less important than interspecific differences (Lewis and Chancy 2008), so in cases where there was no sample from the individual’s village the next closest village was used. Gender-specific average portion sizes for an Amazonian population, calculated by Passos et al. (2008), (125g for women and 190g for men) and the number of fish meals per week reported in the questionnaire were used to calculate the amount of mercury consumed each day.

Daily Hg intake for women = (fish meals per week * Mean Hg concentration of commonly eaten fish (μg/g) * 125 g) / 7

Daily Hg intake for men = (fish meals per week * Mean Hg concentration of commonly eaten fish (μg/g) * 190 g) / 7

Hair analysis. Hair is commonly used as a bioindicator of methylmercury (MeHg) in humans. Since Hg binds to hair and since hair grows approximately 1cm/month, the first cm from the root represents MeHg exposure in the month that the sampling took place (Saitoh et al. 1967; Clarkson et al. 1988). Samples of hair were taken after administering the questionnaire. A small locket of hair was cut at the root. The hair was stapled at the base and stored in plastic bags. Analysis of total mercury and inorganic mercury in hair was carried out at the First Nations and Inuit Health Branch Laboratory (FNIHBL), Health Canada in Ottawa using cold vapour atomic fluorescence spectrometry (CVAFS). Laboratory technicians were kept blind to the samples. The detection limits were 0.006 μg/g for total Hg and 0.004 μg/g for inorganic Hg. Three blanks and one standard (SCP Science) were included every 30-60 samples.

Statistical Analysis. Descriptive statistics on sex, age, ethnic group, schooling and alcohol and cigarette use are presented. Tukey’s HSD multiple mean comparisons was used for testing differences between percent of organic mercury, which was normally distributed. The distribution of hair-mercury (HHg)

concentrations was skewed (Skewness=1.58, Kurtosis=3.15); therefore, non- parametric tests were used where appropriate; otherwise, the log HHg concentration was used. The Mann-Whitney U test was used to test for differences between men and women. The Kruskal-Wallis Test of rank sums was used to test for differences in mercury levels between the months of the year, ethnic group, river and community. A Linear Regression Model was built to describe the HHg concentration in the study population. Since the observations were found across villages and observations from the same village tend to share similar unobservable characteristics that could bias usual ordinary least squares estimates, the data was clustered on village (Moulton 1990). The cluster command corrects for such potential intra-class correlation of the errors. Statistically significant results at P- values of ≤ 0.1, 0.05 and 0.001 are presented. Statistical analysis was performed in Jmp 5.0.1a (SAS institute) and STATA 10.0.

4.3 Results

4.3.1 Hair-mercury Concentrations in the Study Population Fifty percent of the sample population was comprised of women. When divided by river, roughly half were women. When divided by community, most villages had an equal gender balance except Peruanito (35% women) and Añangu (70% women). Key socio-demographic characteristics of the study population are displayed in Table 4.1. Age ranged from 15 to 87 (mean: 36 ± 13.1; median: 33.5). The average years of schooling for the population was equivalent to elementary level (mean: 5.6 ± 4.1 years). Only two people were smokers and most people in most communities reported consuming alcohol.

Table 4.1: Characteristics of the study population by river in the Andean Amazon.

Corrientes River Napo River Pastaza River Characteristic Women Men Women Men Women Men N % N % N % N % N % N % Age 15-24 yrs 10 33 6 17 6 16 2 6 12 43 3 11 25-34 yrs 10 33 11 31 14 37 15 44 6 2 9 33 35-44 yrs 5 17 7 20 11 29 9 27 5 18 8 30 45-54 yrs 4 13 6 17 4 11 4 12 1 4 3 11 ≥ 55 yrs 1 3 5 15 3 8 4 12 4 14 4 15 Ethnic Group Achuar 13 43 14 40 0 0 0 0 0 0 0 0 Kichwa 2 7 2 6 37 97 34 100 26 93 25 93 Mestizo 6 20 8 23 0 0 0 0 2 7 2 7 Shuar 0 0 0 0 1 3 0 0 0 0 0 0 Urarina 9 30 11 31 0 0 0 0 0 0 0 0 Schooling None 14 48 12 35 3 9 1 3 8 33 4 18 ≤ 6 yrs 14 48 16 47 23 66 16 52 11 46 11 50 ≥ 7 yrs 1 3 6 18 9 26 14 45 5 21 7 32 Alcohol user 26 87 32 91 32 84 32 97 12 43 19 70 Smoker* 0 0 2 6 0 0 0 0 0 0 0 0

Notes: *Many of the men smoke when cigarettes are available, perhaps once a month. .

Hair samples for a subset of the women participants on the Corrientes River (n = 6) and the Pastaza River (n = 6) were cut into 12 one centimetre long segments beginning at the root. Each centimetre was analysed for Hg separately. Since hair grows roughly one centimetre per month, sequential analysis indicates whether there are significant differences in Hg intake according to season. There were no significant differences in hair-mercury (HHg) levels in these centimetres in either the Corrientes River (Kuskal-Wallis, P = 1) or Pastaza River communities (Kuskal-Wallis, P = 0.859). Previous analysis had already shown that there are no seasonal differences in mean HHg concentrations in the Napo River populations (Webb et al. 2004). Since mercury levels do not differ significantly according to season, the average of the first two centimetres of hair was used for all subsequent analysis.

The percentage of organic mercury ranged from 83 to 100% (mean: 91%). The percentage of organic mercury in San Carlos (94%) was significantly higher than the other communities using Tukey’s HSD multiple mean comparisons. Total- mercury concentrations were used in all further analysis as this has previously been proposed as the most accurate Hg-species from hair samples (Berglund et al. 2005).

No differences were found in HHg levels between men (mean: 5.70 μg/g) and women (mean: 5.93 μg/g) when the entire study population was examined (Mann- Whitney U, P = 0.84) nor when individuals from each of the rivers and communities were considered separately. No significant differences were found between HHg levels in the different ethnic groups (Kichwa, Shuar, Achuar, Urarina, and Mestizo) overall, within rivers or within communities. No difference was noted when the data were stratified for sex. Log HHg levels were not related to age in the overall population (R2 = 0.0004, P = 0.78) nor on the Napo River (R2 = 0.004, P = 0.61) or the Pastaza River (R2 = 0.0003, P = 0.9). On the Corrientes River, log HHg levels increased significantly with age (R2 = 0.08, P = 0.02). Hair- mercury concentrations were significantly negatively associated with education

(years) when all the data were pooled (R2 = 0.03, P = 0.02), but not when examining each river separately. In most communities, all or nearly all participants were agriculturalists. The community of Añangu, however, owns a community operated ecolodge. In this community they self-identified as agriculturalists or hotel workers. There is a significant difference in the HHg concentration between agriculturalists (mean: 4.65 μg/g) and hotel workers (mean: 2.86 μg/g) (Kuskal-Wallis, P = 0.05) in Añangu (see also below).

Significant differences exist between mean HHg concentrations in the three rivers (Kruskal-Wallis, P < 0.0001) (see Figure 4.2 and Table 4.2). The individuals on the Pastaza River have the highest levels of mercury in their hair (mean: 9.6 μg/g, median: 8.4 μg/g, range: 3.5 to 24.8 μg/g), followed by those on the Corrientes River (mean: 5.6 μg/g, median: 5.1 μg/g, range: 1.9 to 17.3 μg/g) and, finally, the Napo River (mean: 3.1 μg/g, median: 2.4 μg/g, range: 1.1 to 9.1 μg/g). Significant differences also exist between mean HHg concentrations in the eight communities (Kruskal-Wallis, P < 0.0001) (see Figure 4.2 and Table 4.2). Using the Tukey’s HSD multiple mean comparisons on the logged data, five significantly distinct categories emerge (A: Loboyacu and Alianza Capahuari; B: Alianza Capahuari and Peruanito; C: Peruanito, Copal and Nuevo Paraiso; D: Copal, Nuevo Paraiso, and Añangu; and E: Palma Roja and San Carlos).

Figure 4.2: Hair-mercury concentrations (μg/g) by river basin and community. Horizontal line represents the grand mean.

A significant difference was found in the number of fish meals consumed (see Table 4.2) by the sample populations of the different rivers and communities (Kruskal-Wallis, P < 0.0001). No significant difference was found in the number of fish meals eaten per week between men and women in the total population (Mann-Whitney U, P = 0.12). A significant difference was found in the weight of the fish caught in each of the rivers and communities (Kruskal-Wallis, P < 0.0001) (see Table 4.2). The largest fish were caught in the Pastaza River basin, followed by the Corrientes and, finally, the Napo. The class of fish most frequently eaten in each of the rivers (piscivore vs. non-piscivore) was significantly different (Pearson, P > 0.0001). Respondents from San Carlos unanimously reported eating piscivores most frequently, whereas in the other communities responses were divided between piscivores and non-piscivores. People who reported eating non-piscivores had higher HHg concentrations (mean: 6.64 ± 4.6 μg/g) than those who reported eating piscivores most frequently (mean: 4.9 ± 3.3 μg/g) (Mann-Whitney U, P = 0.004).

Daily Hg intake was calculated for each individual and compared across regions (see Table 4.2). There was a significant difference in the daily Hg intake in the three rivers and eight communities (Kruskal-Wallis, P < 0.0001) (see Figure 4.3). The Tukey’s HSD multiple mean comparisons test shows that the respondents on the Napo River have a significantly lower daily Hg intake than the respondents on the Corrientes and the Pastaza rivers.

Table 4.2: Mean hair-mercury concentration (μg/g), number of fish meals per week, mean weight of fish caught in location (g), class of fish most commonly eaten (%), and mean daily Hg intake (μg/day) in the three rivers and eight communities.

River Mean hair- Mean fish meals Mean weight of Piscivore as most Mean daily Hg Community mercury (μg/g) per week (n) fish caught (g) common fish (%) intake (μg/day) (range) (n) (range) Corrientes 5.6 (1.9-17.3) 3.8 (65) 247.8 (105) 38 12.2 (2-37.8) Peruanito 6.6 (2.4-14.8) 4.3 (20) 286.1 (40) 24 15.3 (2.7-37.8) Copal 5.5 (2.6-17.3) 5.1 (25) 209.8 (61) 33 12.7 (3.2-29.5) Nuevo Paraiso 4.8 (1.9-10.5) 1.9 (20) 445.0 (4) 57 8.5 (2-23.4) Napo 3.1 (1.1-9.1) 2.7 (71) 209.3 (74) 65 5.4 (0.06-21.2) Palma Roja 2.9 (1.1-8.8) 1.6 (29) 127.5 (26) 28 5.7 (0.1-21.2) San Carlos 2.4 (1.1-9.1) 5.3 (22) 45.2 (25) 100 6.9 (0.8-17.1) Añangu 4.2 (1.6-7.9) 1.3 (20) 480.2 (23) 85 3.1 (0.06-18.1) Pastaza 9.6 (3.5-24.8) 7.1 (55) 368.5 (132) 33 14.1 (3.3-51.9) Alianza Capahuari 8.0 (3.5-17.6) 7.5 (27) 395.2 (56) 50 16.5 (7.3-43.1) Loboyacu 11.2 (4.4-24.8) 6.6 (28) 348.9 (76) 17 11.9 (3.3-51.9)

Figure 4.3: Daily mercury intake (μg/day) by river basin and community. Horizontal line represents the grand mean.

A linear regression model was constructed to examine which demographic and dietary factors explain observed differences in HHg concentrations. Sex, age, ethnicity, education, and daily Hg intake were considered as explanatory factors (see Table 4.3). Log HHg concentration was the dependant variable (n=190). The model was clustered according to community because of important demographic and dietary differences between communities. Fourteen percent of the variation is explained by this model. Three factors – education, ethnicity, and daily Hg intake – were significant. No colinearity was found between daily Hg intake and education (Pearson correlation coefficient = 0.04; P = 0.58) or age (Pearson correlation coefficient = -0.02; P = 0.77). Age is negatively correlated with education (Pearson correlation coefficient = -0.42; P < 0.001); the older the person, the less likely they are to have gone to school.

Next, a linear model using daily Hg intake as the dependant variable and demographic and dietary factors as covariates was constructed (see Table 4.4). The model was again clustered according to community. Sixty-three percent of the variation in daily Hg intake can be explained by this model, in which only the dietary factors – Hg concentration in the most commonly eaten fish and number of fish meals per week – are significant. No colinearity was found between number of fish meals eaten per week and education (Pearson correlation coefficient = -0.008; P = 0.91) or age (Pearson correlation coefficient = -0.12; P = 0.1). Mean Hg in the most commonly eaten fish is not correlated with either age or education, but is significantly negatively correlated with number of fish meals (Pearson correlation coefficient = -0.2; P = 0.005).

Table 4.3: Total hair mercury concentrations (μg/g) (log-transformed data) and covariates in the Andean Amazon: results of a clustered linear regression analysis.

Covariate Coefficient (t ratio) Constant 2.1 (8.38) Demographic factors Sex (0 = male; 1 = female) -0.09 (0.94) Age -0.003 (0.57) Education (years) -0.03 (1.9)* Ethnicity (0 = Mestizo, 1 = Amerindian) -0.43 (2.76)** Dietary factors Daily Hg intake (μg/day) 0.02 (2.59)** R2 0.14 F 4.00 P(F) 0.049 Number of observations 190

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05.

Table 4.4: Daily Hg intake (μg/day) and covariates in the Andean Amazon: results of a clustered linear regression analysis.

Covariate Coefficient (t ratio) Constant -8.13 (1.66) Demographic factors Age 0.07 (1.62) Education (years) 0.15 (1.24) Ethnicity (0 = Mestizo, 1 = Amerindian) -0.87 (0.55) Dietary factors Mean Hg in common fish (μg) 46.77 (2.14)* Fish meals 2.38 (10.34)*** R2 0.63 F 36.54 P(F) 0.0001 Number of observations 190

Notes: t ratios are in absolute values * p(t)≤0.10. *** p(t)≤0.01.

4.3.2 Change in Hair-mercury Concentrations in Residents of a Village with Increased Work Opportunities over the Period 2002- 2006 A community owned and operated hotel, the Napo Wildlife Center, went into full operation in the community of Añangu in 2003, giving many of the residents work opportunities. When the people from this community who contributed hair in both of the sampling sessions (2002 and 2006) are considered (n = 10) in a matched pairs analysis, a significant difference exists between the HHg levels between the two years (see Table 4.5). Since there are so few people in the matched pairs analysis, non-parametric methods were used as well. The difference between 2002 HHg concentrations and 2006 HHg concentrations was calculated for each individual. Subsequently, the mean of this change in HHg was tested for difference from zero using the Wilcoxon Signed-Rank test and found to be significantly different (signed-rank = 27.5, P = 0.002). The mean HHg level for these ten people fell by a little more than half from 2002 (mean: 9.8 μg/g) to 2006 (mean: 4.6 μg/g) (see Figure 4.4). Number of fish meals also decreased; however, the size of the fish most frequently consumed rose (see Table 4.5). When residents who had remunerated work at the hotel in 2006 (n = 5) are compared with residents who did not work at the hotel (n =15) there is also a significant difference in the HHg concentrations (Mann-Whitney U, p = 0.05) (see Figure 4.5). However, no significant difference in the frequency of fish meals per week was noted between these two groups (Mann-Whitney U, P = 0.8). Overall, in the community of Añangu, mean HHg decreased by almost half between 2002 (mean: 7.9, median: 6.9, range: 0.6-18.7 μg/g, n = 24) and 2006 (mean: 4.2, median: 6.6, range: 4.4-7.1 μg/g, n = 20). This difference is significant (Mann-Whitney U, P = 0.016). If the respondents who reported a family member working in 2006 are excluded (n = 15), there is no longer a significant difference between the respondents of 2002 (mean = 7.9 μg/g, n=24) and those who were not affiliated with the hotel in 2006 (mean = 5.0 μg/g, n=5).

Table 4.5: Matched Pairs analysis of hair-mercury concentrations (μg/g), number of fish meals per week and weight of most commonly eaten fish for 2002 and 2006, Añangu, Ecuador.

Year P Δ Change 2002 2006 Hair Hg (μg/g) 9.8 ± 3.5 4.6 ± 1.6 0.0002 -5.2 (-53%) Fish meals / week 4.8 ± 4.3 0.78 ± 0.9 0.04 -3.8 (-84%) Weight of common fish (g) 267 ± 156 347 ± 177 0.11 80.1 (+23%)

100

Figure 4.4: Hair-mercury concentrations in the years 2002 and 2006 in 10 matched residents of the community of Añangu, Ecuador. Horizontal line represents the grand mean.

101

Figure 4.5: Hair-mercury concentrations in 2006 in residents of the community of Añangu, Ecuador, who had remunerated work (Hotel) and those who did not. Horizontal line represents the grand mean.

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4.3.3 Perception of Quality of Fish Open ended questions on people’s perception of fish, fishing and contamination provide insight into local environmental changes. The concerns expressed by respondents revolved particularly around two environmental problems: activities of the oil companies and overfishing. People remarked that the presence of oil companies has led to a decrease in the number of fish. “The impact of the [oil] companies is that now there aren't so many fish because of transportation and spills” (Añangu). Changes in the quality of fish were also observed. “One can't tell the difference between the flavours of the fish. Further upstream they have a different smell because of the contamination” (Alianza Capahuari) and “When you put the fish from the lagoon in the fire they become dry and break because they have petroleum in them. They are skinny” (Copal). People also commented on how this decrease in fish has affected their diet: “Before there was an abundance [of fish]. There was no petroleum. Then there was a spill and now fish is scarce. There is only enough for breakfast or supper. Before we could fish with a harpoon, now this is no longer possible” (Alianza Capahuari) and “When fish are caught in the net they are black and hurt for no apparent reason. We believe that we can become contaminated if we eat them so we cut off [bad] parts. We eat less fish now because of the petroleum” (Palma Roja). Overfishing was also a concern for some people. “Before there were more fish; there were big boquichico, sabalo and zungaro. The fishing is worse because there are so many people now. People come from downstream in pequepeque (a small boat) and take away the fish” (Loboyacu) and “…there aren't fish like there used to be. They're getting scarce. Now you have to go fishing, bring back your catch, eat, and then you have to go out fishing all over again” (Loboyacu).

Since not everyone had an opinion on these topics, we could not perform statistical analysis on this data. However, by examining the proportions of people who mentioned one of two concerns (oil contamination or overfishing) we note some interesting trends. In two of the communities on the Corrientes River (Peruanito and Nuevo Paraiso), 100% of people who responded to these questions

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mentioned something related to oil contamination and in the third community (Copal), six of the seven comments concerned oil while the final comment pertained to overfishing. On the Pastaza River, all five comments in Alianza Capahuari, a community close to oil activities, focused on contamination whereas in Loboyacu, situated far from oil activities, residents were more concerned about overfishing (n=4) than oil (n=2).

Comments varied more on the Napo River. In San Carlos, in the heart of an oil production field, all comments (n = 3) revolved around oil, whereas in Palma Roja a community at a distance from oil exploitation, comments were split roughly half and half between oil (n = 3) and overfishing (n = 2). In Añangu, most comments were related to competing factors for time (hotel, n = 9); however, one person mentioned each of oil and overfishing as causes of a decrease in fish consumption. No one in this community mentioned knowledge about mercury contamination from our previous trip as a factor influencing their decision to reduce fish consumption.

4.4 Discussion Three main findings emerge from these results. First, the mean HHg concentrations in several of the communities studied here are high. Concentrations were found to be dependant on daily Hg intake which in turn is dependant primarily on the quantity of fish consumed. The high Hg concentrations found in commonly eaten fish species combined with a high frequency of fish consumption exposes people in some of the communities to mercury at levels higher than recommended. Second, this study suggests that a change in livelihood from agriculture and fishing to remunerated work reduces HHg levels. Third, people appear to be eating less fish as a result of petroleum contamination.

The levels of mercury detected in the hair of indigenous populations in our sample fall within the range of previous studies conducted among Amazonian indigenous

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groups (for a review see Passos and Mergler, 2009). Kehrig and colleagues (1997) observed a lower mean hair mercury concentration – 3.32 μg/g – in a group of Yanomama who only consume fish occasionally (p.21). Kayapó hunters, living along the Fresco River, where gold mining activities had only just begun, had a mean hair mercury concentration similar to that found in this study population – 8.0 μg/g (Barbosa et al. 1995, p.114). A study among the Pakaanóva (Rondônia), a gold mining area, also found similar mean mercury in hair samples (8.37 μg/g), but some individuals presented extremely high levels and one child’s hair reached 83.89 μg/g (de Oliveira Santos et al. 2003, p.199). The Parakanã, living near a severely contaminated reservoir, the Tucuruí (Pará), consume on average two fish meals per week and were found to have lower levels of mercury (mean: 8.5 μg/g) than neighbouring fish-eating, non-indigenous communities (Leino and Lodenius 1995, p.123). Soares de Campos and colleagues (2002) found lower levels of mercury (median: 6.06 μg/g) in indigenous people’s hair in Rhodonia State (p.159).

The highest levels of mercury in Amerindian people of the Amazon have been found in the Tapajós River Basin. A study conducted in the headwaters found a mean mercury concentration of 12.7 μg/g among the Kayabi, who consume approximately 110 g of fish per day and 3.4 μg/g among the Munduruku who reported eating 30 g per day (Dórea et al. 2005, p.209). Higher levels of mercury were found the in the hair of the Munduruku and Apiaká people (mean: 34.2 μg/g) living at the confluence where the Tapajós River begins, a region with substantial gold mining (Barbosa et al. 1997, p.3).

Few studies have been conducted on mercury levels in Amazonian indigenous people outside Brazil; but the studies that have been conducted show similar levels to those reported in the present study. A study along the Beni River, Bolivia, found that the mean HHg concentration in a fish-reliant group, the Essajas, was significantly higher than in gold miners (9.81 vs. 0.28 μg/g) (Maurice-Bourgoin et al. 2000a, p.73). In the French Guiana a study conducted

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among the Wayana community found a mean similar to that which we found on the Pastaza River (mean: 11.4 ± 4.2 μg/g) (Frery et al. 2001). Another study in French Guiana evaluated HHg concentrations among children from several Amerindian communities (mean: 5.1 μg/g) (Cordier et al. 1998, p.3). In a mixed population of children in Ecuador, including Saraguro Amerindians, and living in a gold-mining region of the Andean foothills the mean level of mercury in hair was 6.0 μg/g (Counter et al. 2005, p.134).

The observed HHg concentrations in the present study are strongly related to the community in which the individual lives. But what is it about each of the communities that makes the concentration of mercury in hair so different? Our linear regression indicates that daily Hg intake, education and ethnicity influence mercury levels. Daily Hg intake is in turn strongly influenced by number of fish meals eaten per week and less so by the Hg concentration is the most commonly eaten fish. Environmental, geographic and socio-economic factors appear to be contributing to the observed difference through their impact on the size, trophic level and quantity of fish consumed in each of the communities.

We expected to see HHg levels vary with the quantity of fish consumed. The most highly significant variable in the model of log HHg was daily Hg intake, itself reliant on the number of fish meals consumed per week. How much fish people eat is determined by a variety of geographic and socio-economic factors. Communities located near to a lagoon would be expected to eat more fish than communities that are not (San Carlos, Palma Roja and Nuevo Paraiso), since fish are more abundant in lagoons and fishing is, therefore, less time consuming in lagoons than on the rivers. Indeed, two of the communities without a local lagoon, San Carlos and Palma Roja, have the lowest HHg levels. Although the participants in San Carlos report eating five fish meals per week, they are most likely eating smaller portions since the size of the fish available to people in this village is significantly smaller than in other villages.

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Two socio-economic factors influencing the quantity of fish consumed per week are access to markets (Webb 2004) and livelihood activities that compete with fishing for time. Many people from Palma Roja travel to the city of Coca every Sunday to sell produce, often returning with a chicken for supper, and people in San Carlos live 45 minutes by bus from Coca. Some residents in Añangu work at the Napo Wildlife Center and noted that a lack of time for fishing contributed to their decreasing consumption of fish. Further, fishing has been outlawed in the Añangu lagoon since the inception of the hotel to encourage wildlife into the area.

Another factor influencing the amount of fish consumed is the perception of the quality of the fish and the health of fish stocks. In general, people in communities close to oil operations expressed concern about the health of fish and fisheries in the face of contamination more frequently than those in communities far from oil wells. In two communities far from commercial fish markets but that have been undergoing oil exploitation for the past 30 years, all responses to open ended questions pointed to concern over contamination from oil. In the community closest to a large fish market, San Carlos, but also closest to oil wells, all comments pertained to contamination from oil. Interestingly, the two communities with the lowest HHg levels had the lowest response rate on this question, perhaps because fishing is comparatively less important to these people.

The amount of mercury in fish is known to be influenced by its size, with larger fish having higher concentrations (see Chapter 3). The weight of fish caught in each community differed significantly. Factors influencing the size of the fish are largely related to where the fish are caught. Communities that fish primarily in streams, such as San Carlos, would be expected to catch smaller fish than those that fish in a lagoon or the river. People’s access to resources and time constraints can also influence the size of fish. Catching large catfish in the river is time consuming, unpredictable, and, with no refrigerators, unnecessary.

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Piscivores are known to have higher concentrations of mercury than herbivores (see Chapter 3). People who reported eating non-piscivores, however, had higher HHg concentrations than those who reported eating piscivores most frequently. This discrepancy could be due to the fact people who regularly practice fishing with a net, thereby catching more herbivores, also eat more fish. This is supported by the finding that the mean Hg concentration in the most commonly eaten fish is negatively associated with the number of fish meals consumed per week, so the people who eat fish most often tend to eat fish with less mercury. This would probably be because non-piscivores are caught with a net and fishing with a net gives a higher yield. Our data do not show that people who eat non-piscivores eat fish more frequently but they could be eating larger portions. Finally, the variability in the size of piscivores is higher than for herbivores. Whereas piscivores can be substantially bigger than herbivores, in the community of San Carlos, where they reported unanimously eating piscivores, they fish primarily in streams as opposed to the river or a lagoon and hence their fish are substantially smaller.

Education is a common determinant of HHg concentrations, largely through differences in diet preference and access to alternatives (Passos et al. 2008). There was no relationship between number of fish meals people reported eating per week and education (years). While people with less schooling do not eat fish more frequently, they may eat larger portions of fish, since they are not substituting with other animal protein. It could also be that people with less education use simpler fishing technology due to lower income or fewer assets. Both nets and hooks must be bought. Fishing with a harpoon in streams or shallow water, a simple method, would predispose the fisher to catch piscivores, especially Hoplias malabaricus. Lagoons, where herbivores are often caught outside of the spawning season, are often situated far from the village and if one does not own a motor boat the trip can be lengthy.

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Ethnicity (mestizo vs. Amerindian) was found to be significantly associated with HHg. Ethnicity probably influences the amount, type and size of fish people eat. For example, the Urarina recently established the community of Nuevo Paraiso. Less than ten years ago they lived in forest communities where they would have had less access to fish and so game is relatively more important in their diet even though they now live along the Corrientes River. Indeed, the Urarina reported eating 1.9 fish meals per week compared to 4.5-5 fish meals per week for other groups. Fishing is an art and experienced fishers catch more fish than those who have less experience. New evidence is also suggesting that genetic characteristics and the effects of other components in the diets of some ethnic groups cause them to display lower mercury levels in hair than what would be expected (Canuel et al. 2006).

Age was not a significant covariate in the overall model but it was significantly related to HHg concentrations along the Corrientes River. This could be because the Corrientes populations are in a period of transition. Considering that roads were built to the Napo River in the 1970s, giving local people greater access to market goods, it seems likely that these populations reduced their fish consumption some time ago; hence, elders have also made the change. On the Pastaza River, fish consumption remains high in all age categories. It could be that the younger generations of riparians living on the Corrientes River are presently reducing their fish consumption either due to the perception that it is no longer safe for consumption, as evidenced by the qualitative data, or because of greater access to markets, while older people are retaining a traditional diet based on fish protein.

Regulatory agencies analysed several longitudinal, neurodevelopmental toxicity studies and estimated that the amount of mercury intake without appreciable risks ranges from 0.1 to 0.23 µg/kg/day (Mergler et al. 2007). While the weight of each individual in the study population was not recorded, if average weights for men and women from a similar study conducted in the Amazon are used (52 kg for

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women and 60 kg for men) (Passos et al. 2008) then the daily Hg intake per body weight for this study population ranges from 0.001 to 0.86 µg/kg/day. The fact that the upper range in this study surpasses the daily mercury intake without appreciable risks by 66% is cause for concern.

Most people in the study population are agriculturalists who cultivate crops for their own consumption. In the community of Añangu, however, many people work at the Napo Wildlife Center. Our results show that those people who work in the hotel have significantly less mercury in their hair than those who do not. Respondents from Añangu reported that they no longer have the time to fish because they are working. It has also been observed that community members eat meals at the hotel. Our results show that the levels of HHg decreased by almost half in the community of Añangu between 2002 and 2006 (the Napo Wildlife Center was opened in 2003). Although it is possible that the levels decreased because we had been in the village in 2003 to return the results of the first study to the participants, the evidence suggests that most of the change is rooted in the fact that residents of this village have shifted their livelihoods from subsistence based farming and fishing to remunerated work. All members of the community were invited to the workshop that we held and there is no reason to believe that the advice we gave would have been heeded to a larger extent by those working in the hotel. It appears that a change in livelihood can alter HHg levels through competing with fishing for an individual’s time. Wunder (2000) also found that people participating in ecotourism activities in the Cuyabeno Reserve of the Ecuadorian Amazon had less time to dedicate to hunting.

4.5 Implications The Andean Amazon is a region that has been little studied to date, but which, due to its proximity to the Andes, high levels of deforestation and dependence on oil extraction, is at risk of mercury accumulation in the aquatic food chain. The results presented here show that communities reliant on fish as a protein staple, have high levels of HHg. Our results also show that HHg levels are dependent on

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education, ethnicity, and daily Hg intake. Daily Hg intake was strongly associated with the number of fish meals consumed per week and less so with the average Hg concentration in commonly consumed fish species. The size, trophic level and quantity of fish consumed are reliant on socio-economic, geographic and environmental factors. Livelihood changes that led people away from subsistence farming and fishing and toward remunerated work were shown to have a strong impact on fish consumption leading to a decrease in mercury levels.

Mercury is imperceptible but crude oil is not. An important finding of this study is that environmental contamination from the oil industry is influencing people’s perception of the health of their fisheries. People who live closer to oil operations mention more frequently that they are concerned about contamination than people who live far away. Petroleum contamination includes many toxic substances, such as hydrocarbons, mercury, lead, cadmium and other heavy metals. Very little is known about the synergistic health impacts of this combination of contaminants. Local people intuit that the pollution they see and smell is not healthy for them or their fisheries. People in this region are curbing their consumption of fish due to the changes in the smell, flavour and appearance that they are observing in fish. Further, if suggestions made by some local people and studies that fish stocks are declining due to spills, river transportation, and physical changes to the environment (damming streams, etc.) are accurate, it may be more difficult to fish as a result of the presence of oil companies.

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Chapter 5: Mercury Concentrations in Urine of Riparian Communities Living Near Oil Fields in the Andean Amazon (Peru and Ecuador)

5.1 Introduction Mercury is a global pollutant of concern due to its toxic effects and persistent nature. Fossil fuel emissions, dental amalgams, thermometers and artisanal gold mining release elemental mercury into the environment. Mercury discharges to the environment from industry have decreased in recent years due to strict regulations, with the notable exception of the production and processing of hydrocarbons (Wilhelm 1999). Crude oil, sludge and production waters from the extraction process contain mercury (Wilhelm 1999). Crude oil arriving to the United States from Ecuador contains on average 1.8 μg/kg of mercury and the average for South America is 5.3 μg/kg (Wilhelm et al. 2007, p.4512). This is lower than levels reported for Asia (220.1 μg/kg), but higher than those reported for Africa (2.7 μg/kg), the Middle East (0.8 μg/kg), United States (4.3 μg/kg) and Canada (2.1 μg/kg) (Wilhelm et al. 2007, p.4512). Much of the initial mercury, however, adheres to substrates in holding reservoirs and pipelines before reaching its destination (Wilhelm et al. 2007). Indeed, mercury has been regarded as one of the impurities in petroleum responsible for the deterioration of petroleum installations (Bloom 2000b). Production waters are thought to contain more mercury than the crude oil itself, but no studies have been conducted to quantify precisely how much (Wilhelm 2001).

Elemental mercury can form stable bonds with organic matter in soils and with hydrocarbons in co-contaminated sites (Renneberg and Dudas 2001). A study in Nigeria found that Hg levels in soils were higher near a gas plant than along a pipeline, but that levels did not exceed background levels (Iwegbue et al. 2006). Studies conducted after a spill in Nigeria showed that metal levels were higher in contaminated soils than control sites (Osuji and Onojake 2004; Osuji and Onojake 2006). Several studies show that spills or routine extraction practices lead to Hg

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contamination of the surface soil (Haidouti 1991; Osuji and Onojake 2004), owing to the fact that metals generally do not penetrate soils. Moreover, a study examining the impacts of river bank deforestation on mercury levels showed that deforestation – often provoked by petroleum extraction activities such as road construction – leads to the erosion of top-soils and the leaching of the mercury contained in these surface soils into aquatic environments (Roulet et al. 2000; Mainville et al. 2006).

A study on metal levels in the North Sea near abandoned drilling platforms found a positive correlation between barium, another heavy metal, and total oil in sediments (Breuer et al. 2004). Research on Hg levels near offshore oil rigs in Brazil was inconclusive due to the high variability in samples (Lacerda et al. 2004). Another study conducted in the coastal waters of Brazil showed that levels of trace metals increased after drilling operations but not to a level significantly different from control sites (Rezende et al. 2002). Researchers evaluating the levels of active Hg evasion from a major oil spill off the coast of Korea have found that sites closer to the spill had significantly higher levels of gaseous mercury than those further away, yet the reference site (one block away from the spill) also had elevated mercury levels (Pandey et al. 2009). Further, analysis one month after the spill showed a significant drop in mercury at all sites, yet the levels at the site of the spill were still higher than those farther away.

A study after the Prestige oil spill off the coast of Spain found that seabirds were contaminated in Hg (Perez-Lopez et al. 2006). Another study, however, did not find an increase in Hg levels (Carbonell et al. 2007) and, in fact, one study reported a decrease in Hg in a predatory bird species, which they attribute to the birds being forced to eat lower on the trophic chain following fish die-offs (Sanpera et al. 2008). An experimental study showed that fingerlings exposed to petroleum refinery effluent accumulated metals to a thousand times those in the exposure medium (Onwumere and Oladimeji 1990, p.123). Metal levels in mussels near an abandoned offshore operation were not found to be higher,

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despite the fact that core sediments did show enhanced levels of metals (Phillips et al. 2006). Bou-Olayan et al. (1995) suggest that the increased levels of metals that they found in pearl oysters in 1992 compared to 1990 could be due to the 1991 Gulf War oil spill. However, Al-Muzaini and Jacob (1996) report that sediment concentrations were not different from base-line levels after the spill.

Very little is known about the amount of mercury or other toxic agents released in open flares, a practice used to burn off excess gas during petroleum extraction; however, it is widely accepted that the burning of fossil fuels is a major anthropogenic source of mercury into the atmosphere (National Research Council 2000). Mercury concentrations were found to be 10 times higher in the upper layers of sediment cores taken from a lake situated near to a coal burning plant in Texas (Menounou and Presley 2003). Most studies on this topic evaluate the mercury released from coal or natural gas burning electricity plants where flues are used to capture much of the mercury contained in the gases released (on average 75% of the mercury is removed from Dutch power plants and it is possible to filter 90% (Meij et al. 2002)). Studies in Kuwait and Saudi Arabia conducted after the open burning of oil wells during the first Gulf War have not been conclusive in quantifying the contamination of the atmosphere, aquatic environments and desert ecosystems by metals released from the combustion of crude oil (Al-Houty et al. 1993; Husain 1994; Sadiq and Mian 1994; Osman 1997).

Inorganic mercury, as measured in urine or blood, is usually indicative of exposure to elemental mercury in vapour form (ATSDR 1999). Elemental mercury is much more readily absorbed by the lungs than the skin (Hursh et al. 1989). Urine has been regarded as the appropriate biomarker to consider when examining chronic exposure to mercury vapour, whereas blood captures peak exposures (Barregård 1993). The half life of urinary Hg is 40 to 90 days (Clarkson 2002). A review article summarizes values of mercury in the urine of control populations, ranging from 0.03 to 42 μg/l (Tsuji et al. 2003). The upper limit for

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unexposed populations set by the WHO is 10 μg/L (WHO 1991). Levels lower than this (around 3 μg/L as a maximum) have been recommended for children (Tsuji et al. 2003).

Most studies that examine human environmental exposure to elemental mercury consider exposure to gaseous mercury from dental amalgams or in domestic or highly polluted industrial settings. Many studies have established a link between number of dental amalgams and inorganic mercury (for a review see Hanson and Pleva (1991)). Studies on children’s exposure to mercury vapour have tended to focus on broken thermometers and ritualistic uses of mercury (for a review see Counter and Buchanan (2004)). A study in China calculated an intake dose of 0.142–0.161 μg/kg/day of mercury in residents living near a power plant where the atmospheric Hg concentration was 0.5 μg/m3 (Zhang and Wong 2007, p.115). A probabilistic study estimated that coal plants double the upper percentile of exposure to mercury in surrounding communities (Lipfert et al. 1994). No studies on the extent of contamination in humans exposed to unfiltered sources of combusted fuel could be found.

Fewer studies have examined environmental exposure through ingestion or dermal uptake. A very recent study indicates in the abstract that volunteers not wearing protective gear during an oil spill clean-up effort had increased levels of Hg in their urine as compared to those who did use protective devices (Lee et al. 2009b). Tolerable limits of mercury in drinking water have been set at 1 μg/l by the WHO (WHO 1993), but few studies report on exposure through drinking water. A recent study on handling contaminated soils found that as a result of adhesion to carbonates, metal concentrations, including mercury, on the hands were elevated (Siciliano et al. 2009).

The main source of organic mercury in non-occupationally exposed persons is through fish consumption (Clarkson 2002). Fish consumption leads to high levels of methylmercury as measured in blood and hair. Studies conducted in the

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Andean Amazon have consistently associated MeHg levels in riparian populations with fish consumption (Maurice-Bourgoin et al. 2000a; Webb et al. 2004) (see also Chapter 4). Recently, however, some studies have shown that there is a significant relationship between inorganic mercury concentrations and fish consumption (Apostoli et al. 2002; Johnsson et al. 2004; Levy et al. 2004; Passos et al. 2007b). These authors suggest that demethylation of methylated mercury is taking place in the body. On the other hand, the Agency for Toxic Substances and Disease Registry (ATSDR) (1999) maintains that urinary mercury (U-Hg) is less impacted by MeHg in the diet than is blood mercury.

Elemental mercury is primarily absorbed by the lungs (Guzzi and La Porta 2008). Symptoms include cough, dyspnea, fever, tremors, malaise, axonal sensor motor polyneuropathy, gingivitis, delusions, hallucinations and mercurial erythrism (excitability, loss of memory, insomnia, extreme shyness and neurocognitive disorders) (Vroom and Greer 1972; WHO 1991). Inorganic mercury in the body can have negative impacts on the central nervous system and can cause developmental problems in children (ATSDR 1999). Mercury is known to negatively impact the immune system even at low doses and has been suggested as playing a role in the onset of lupus (Yoshida and Gershwin 1993; Sweet and Zelikoff 2001). A study investigating a cluster of lupus cases in a neighbourhood built on an abandoned oil field in New Mexico found that ambient mercury measurements were higher in the homes where lupus cases were identified (Dahlgren et al. 2007). They also observed an increased prevalence of disorders other than lupus including cardiovascular, neurological and respiratory problems. Significant differences in B cells, gamma glutamyl transferase, globulin and serum calcium levels were observed between exposed and non-exposed populations (Dahlgren et al. 2007). The authors implicated a combination of mercury and pristine, a straight chain alkane, emanating from crude oil deposits in these complications (Dahlgren et al. 2007).

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The aim of this exploratory research is to determine the levels of inorganic mercury in the urine of rural, riparian populations in the Ecuadorian and Peruvian Amazon. Linear regression techniques are used to explore associations between these levels and fish consumption, occupation and other socio-demographic characteristics.

5.2 Methods Study Area. The present study was carried out along three white-water rivers in the Andean Amazon (also known as the Upper or Western Amazon): the Corrientes River, Peru, which has been subject to extensive petroleum activity for the past 35 years with an estimated 115,000 barrels extracted per day; the Napo River, Ecuador, which has been undergoing heavy petroleum extraction for the past 45 years reportedly extracts 500,000 barrels per day; and the Pastaza River, Peru, which has seen petroleum activity in the upper reaches of the study area for 35 years and recently signed a prospecting contract for the lower reaches (Loboyacu) (see Figure 1.1). Although there are no marked wet and dry seasons, December to February is relatively drier and May and June are relatively wetter.

In addition to the routine practices that regularly release petroleum and petroleum wastes into the study region and the numerous spills that have occurred over the years, a spill resulting from the collapse of a section of a pipeline passing through Peruanito occurred four and a half months prior to sampling (Aste Daffos 2006). It is not known how many barrels of crude oil were released, but the spill covered an area of 7,820 square metres (92 m * 85 m) and the extent of the direct damage is estimated to be 11,800 m2 (Aste Daffos 2006, p.3). However, because rains can carry the crude oil into adjacent micro watersheds, the area impacted by the spill is estimated to be much larger than this (Aste Daffos 2006). Twelve members of the community of Peruanito and ten from Copal were hired as occasional workers to clean up the spill. Their job consisted in, first, spreading an absorbent (Oclansorb) and then collecting the crude oil into barrels and burning it (Mucushua Vilchez 2006). The workers reported a pungent smell from the

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burning of the crude oil, which made several of them sick (Mucushua Vilchez 2006).

A conservative estimate of the mercury released into the northern Ecuadorian Amazon between 1967 and 1993 is 191 kg. This estimate was calculated using 934 kg/m3 for the density of heavy crude oil, Hurtig and San Sebastián (2004)’s approximation of 30 billion gallons of contamination and the mercury content of Ecuadorian crude oil, 1.8 μg/kg. This is certainly an underestimate considering that the mercury content is higher in waste waters than in crude oil and that this does not take into consideration mercury released in flares. In comparison, it has been estimated that small scale gold mining throughout Brazil has released thousands of tons of mercury (Passos and Mergler 2009, p.S503).

Populations and recruitment. The study was carried out with people in eight villages along the three rivers (Napo River: Palma Roja, San Carlos, Añangu; Corrientes River: Peruanito, Copal, Nuevo Paraiso, and Pastaza River: Alianza Capahuari and Loboyacu) (see Figure 1.1) in 2006. Communities are located at varying distances (0-50 km) from oil infrastructure (either a well or a pipeline). The populations are primarily Amerindian peoples of the Kichwa, Achuar and Urarina nations. Most people practice subsistence agriculture, fishing and hunting; however, some people do work occasionally for the oil companies and/or the tourism industry. All villages have primary school, while in most villages secondary education is attained through visiting teachers. Health services and visits to a dentist are difficult to access due to the cost and distance. Occasional visits to the area are made by NGOs providing health and dental care. On these occasions, dental care consists of removing problem teeth. In all but one of the villages (San Carlos) the nearest city is only accessible by boat.

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invited to participate on a voluntary basis. Questionnaires were administered in a private space in the informant’s home and the sampling was carried out by the individual. The informed consent form was read aloud and participants signed. All adults were eligible and no one incurred reprisal for not participating. No compensation was provided. Ethics approval was obtained from the McGill University Ethics Review Board. No permits were required from the Ecuadorian or Peruvian governments.

Questionnaire. The questionnaire (see Appendix 1) was validated for cultural context in a previous study in the region (Webb et al. 2004). The questionnaire, composed of approximately 35 short questions, was organized into five sections – personal information (age, sex, ethnic group), health (smoking, drinking, health problems), occupation, fishing, and diet (including water). The questionnaire took approximately a half an hour to complete. Since methylmercury is known to come from a fish diet, diet questions focused on the frequency (number of times per week), species and provenance of fish consumed. Work in gold extraction and with petroleum is an important exposure pathway, so the occupational section of the questionnaire focused on these two job descriptions.

Urine sampling. Since this was considered a pilot study, every other person interviewed was invited to provide a urine sample (except when there were more than two people in a household at which point we asked the first person at the next house). Two hundred and twelve people, 15 years of age and older, were invited to join the study by answering a questionnaire. Fourteen people refused. In total, 198 people were interviewed. Of these, 87 were asked to give a urine sample. Four people refused. Six people did not return their urine pot, leaving 77 people who contributed urine samples. One sample did not contain enough urine after other analyses. The total sample population included 76 individuals. For cultural reasons, no women from the Urarina community of Nuevo Paraiso gave urine samples. Samples were collected as a single void, since the participants were not recently exposed to mercury through their work. Samples were kept in a

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polypropylene bottle (Nalgene™), in the dark at approximately -4-0°C while in the field and then at -20°C until analysis.

Sample analysis. Analysis of inorganic mercury in urine samples was performed at the First Nations and Inuit Health Branch Laboratory (FNIHBL), Health Canada in Ottawa using cold vapour atomic fluorescence spectrometry (CVAFS). Laboratory technicians were blind to the location of each sample. The detection limit was 0.279 ppb. Three blanks and one standard (SCP Science) were included every 30-60 samples. Concentrations of creatinine were used to standardize for diuresis. Creatinine analysis was carried out at the Centre de Toxicologie du Québec (CTQ) of the Institut national de santé publique du Québec (INSPQ) using the Jaffe reaction (Microgenics kit #1797) on a Hitachi 917 analyzer. The quantification limit was 0.3 µmol/L (3.3 times the detection limit). Blanks and quality control standards were included in the sequence. The standards were Sigma Creatinine standard Kit part number C361 and QC urine material from MAS Urichem (Thermo), levels L1 and L2. They were included every 10 samples.

Statistical Analysis. Descriptive statistics on sex, age, ethnic group, schooling and alcohol and cigarette use are presented. The data for both U-Hg (μg/g creatinine) and creatinine (µmol/l) were skewed (U-Hg: Skewness = 2.9, Kurtosis = 11.3; Creatinine: Skewness = 1.2, Kurtosis = 0.58), so non-parametric tests were used where appropriate; otherwise the log U-Hg concentration was used. The Mann-Whitney U test was used to test for differences between men and women. The Kruskal-Wallis Test of rank sums was used to test for differences in U-Hg levels between the rivers and communities. A linear regression model was built for the entire study population using demographic, occupational and dietary parameters to describe U-Hg concentrations. Since the observations were found across villages and observations from the same village tend to share similar unobservable characteristics that could bias usual ordinary least squares estimates, the data was clustered on village (Moulton 1990). The cluster command corrects for such potential intra-class correlation of the errors. Additional clustered linear

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regression models were constructed for men and women separately. Statistically significant results at p-values of ≤ 0.01, ≤ 0.05 and ≤ 0.1 are shown. Statistical analysis was performed in Jmp 5.0.1a (SAS institute) and STATA 10.0.

5.3 Results Key socio-demographic characteristics of the study population are displayed in Table 5.1. The median value of U-Hg was 2.0 μg/g creatinine, the mean was 2.6 μg/g creatinine and the range was 0.02-15.6 μg/g creatinine. Forty six of the individuals were men (61%) and 30 were women (39%). We did not observe a significant difference in the levels of U-Hg between men (mean U-Hg = 3.2 μg/g creatinine) and women (mean U-Hg = 2.2 μg/g creatinine) (Mann-Whitney, P = 0.12). When individuals from each of the rivers were considered separately, there was no significant difference between the sexes either. There was a significant difference between U-Hg levels in men and women in only one of the communities: Loboyacu (Mann Whitney, P = 0.05), where women had a greater mean concentration (7.6 μg/g creatinine, n = 3) than men (2.4 μg/g creatinine, n = 7). The highest level found in the study population (15.6 μg/g creatinine) was from a woman in this community. Our results show no significant difference in levels of creatinine between men and women (Mann-Whitney, P = 0.74) (mean creatininem = 6.2 μmol/l; mean creatininew = 5.9 μmol/l). Despite the fact that there are not significant differences in U-Hg between men and women in the majority of communities, we stratified for sex in many of the statistical analyses because of important differences in daily activities, leading to different exposure pathways.

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Table 5.1: Characteristics of the study population by river and sex in the Andean Amazon: age, ethnic group, schooling, alcohol use and smoking status.

Corrientes Napo Pastaza Characteristic Women Men Women Men Women Men N % N % N % N % N % N % Age 15-24 yrs 3 33 3 19 2 13 1 7 3 60 1 8 25-34 yrs 4 44 6 38 8 50 6 43 1 20 5 39 35-44 yrs 1 11 3 19 4 25 1 7 1 20 4 31 45-54 yrs 1 11 3 19 2 13 3 21 0 0 2 15 ≥55 yrs 0 0 1 6 0 0 3 21 0 0 1 8 Ethnic Group Achuar 7 78 6 32 0 0 0 0 0 0 0 0 Kichwa 0 0 1 5 16 100 14 100 5 100 13 100 Mestizo 2 22 3 16 0 0 0 0 0 0 0 0 Urarina 0 0 9 47 0 0 0 0 0 0 0 0 Schooling None 3 33 8 44 0 0 0 0 1 33 2 17 ≤ 6 yrs 6 67 2 11 8 57 7 58 2 67 6 50 ≥ 7 yrs 0 0 8 44 6 43 5 42 0 0 4 33 Alcohol user 9 100 18 95 14 88 13 93 3 50 9 69 Smoker* 0 0 1 5 0 0 0 0 0 0 0 0

*Many of the men smoke when cigarettes are available, perhaps once a month.

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Concentrations of mercury in urine were compared according to socio- demographic characteristics of the respondents. No significant differences were found between U-Hg levels in the different ethnic groups (Kichwa, Achuar, Urarina, and Mestizo) overall (Kuskal-Wallis, P = 0.17), within rivers or within communities. Neither was there a difference noted when the data were stratified for sex. Age ranged from 15 to 62 (mean: 35). Log U-Hg levels were not related to age in the overall population (ANOVA, P = 0.32) nor on any of the rivers. The average years of schooling for the population was equivalent to elementary level (mean: 5.9 ± 4.1 years). There is a significant relationship between log U-Hg and education (years) in the overall population (ANOVA, P = 0.059), yet, when separated by river, this relationship is only significant on the Pastaza River (ANOVA, P = 0.11).

Significant differences exist between mean U-Hg concentrations in the three rivers (Kruskal-Wallis, P = 0.04) (see Table 5.2 and Figure 5.2). The people sampled on the Pastaza River have the highest levels of mercury in their urine (mean: 3.2 μg/g creatinine, median: 2.6 μg/g creatinine, range: 0.2 to 15.6 μg/g creatinine), followed by the Corrientes River (mean: 3.0 μg/g creatinine, median: 2.6 μg/g creatinine, range: 0.39 to 10.7 μg/g creatinine) and, finally, the Napo River (mean: 1.9 μg/g creatinine, median: 1.2 μg/g creatinine, range: 0.02 to 9.8 μg/g creatinine). Significant differences also exist between mean U-Hg concentrations in the eight communities (Kruskal-Wallis, P = 0.008). Contrary to the differences between data pooled by river, the community with the highest mean U-Hg concentration – Copal – is on the Corrientes River (mean: 4.83 μg/g creatinine, median: 3.8 μg/g creatinine, range: 1.7 to 10.7 μg/g creatinine) (see Table 5.2 and Figure 5.2).

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Table 5.2: Mean U-Hg concentration, occupational characteristics and dietary characteristics of the study population River Mean U- Mean Approx. Work in Women Surface Mean fish Mean Community Hg (μg/g creatinine distance petroleum with water as meals per weight of creatinine) (µmol/l) to oil company family most week (n) fish caught (SD) (SD) well (men) working common (g) (n) (km) (n, %) for source of company water (%) (n, %) Corrientes 3.0 (2.3) 5.1 (3.5) 10 (53) 7 (88) 100 3.8 (27) 247.8 (105) Peruanito 2.1 (1.2) 4.4 (2.3) 5 6 (100) 3 (75) 100 4.7 (10) 286.1 (40) Copal 4.8 (3.0) 4.6 (2.7) 20 4 (100) 4 (100) 100 4.9 (8) 209.8 (61) Nuevo Paraiso 2.2 (1.8) 6.3 (4.9) 50 0 (0) NA 100 1.9 (9) 445.0 (4) Napo 1.9 (1.8) 6.7 (4.9) 6 (43) 7 (47) 87 2.3 (29) 209.3 (74) Palma Roja 2.3 (3.3) 6.9 (5.8) 15 2 (50) 2 (67) 100 1.7 (7) 127.5 (26) San Carlos 1.2 (0.64) 6.7 (3.8) 0 1 (20) 0 (0) 67 4.6 (8) 45.2 (25) Añangu 2.2 (1.3) 6.5 (5.4) 32 3 (60) 5 (63) 93 1.4 (14) 480.2 (23) Pastaza 3.2 (3.3) 5.9 (5.0) 8 (62) 3 (75) 67 6.9 (18) 368.5 (132) Alianza Capahuari 2.2 (1.5) 8.5 (5.9) 10 5 (83) 2 (100) 25 7 (8) 395.2 (56) Loboyacu 4.0 (4.2) 3.8 (3.2) 100 3 (43) 1 (50) 100 6.9 (10) 348.9 (76)

Note: Mean U-Hg concentration (μg/g creatinine), mean creatinine (µmol/l), approximate distance of community from oil wells (km), men with previous employment with the oil company (number and %), women with family members who have worked for the oil companies (number and %),surface water as most common source of drinking water (%), mean fish meals consumed per week and mean weight of fish caught in community (g) in the three rivers and eight communities.

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Figure 5.2: Mercury concentrations in urine (μg/g creatinine) by river basin and community. Horizontal line represents the grand mean.

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Log U-Hg is significantly positively related to log hair mercury (log U-Hg = - 0,57658 + 0,787059 Log HHg). These measures are related on each of the rivers as well. Hair-Hg was positively associated with the number of fish meals consumed per week (see Chapter 4); however, U-Hg does not display this same trend (ANOVA, R2 = 0.01, P = 0.33) (see also Table 5.3).

A linear regression model with log U-Hg as the dependant variable and age, education, work recovering crude oil from a recent spill, source of washing water, number of fish meals per week, and mean Hg of commonly eaten fish as model effects showed that dietary variables are not significant, whereas, previous work cleaning up a spill and the source of water are (see Table 5.3). Education is also shown to be significant. More highly educated people had less mercury in their urine. There is no colinearity between education and number of fish meals per week (Pearson Correlation Coefficient = 0.03; P = 0.79). Age is negatively correlated with education (Pearson Correlation Coefficient = -0.35; P = 0.0019); the older the person, the less likely they are to have gone to school. Neither age nor education are significantly correlated with number of fish meals (Age: Pearson Correlation Coefficient = -0.03, P = 0.8; education: Pearson Correlation Coefficient = -0.03; P = 0.79). Hg in commonly eaten fish is not correlated with age (Pearson Correlation Coefficient = -0.1, P = 0.36) but is correlated with education (Pearson Correlation Coefficient = -0.26; P = 0.03). Finally, average Hg of most commonly eaten fish is not correlated with number of fish meals consumed per week (Pearson Correlation Coefficient = 0.07; P = 0.56).

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Table 5.3: Concentration of mercury in urine (log-transformed data) and selected covariates: results of a clustered linear regression analysis.

Covariate Coefficient (t- ratio) Constant -0.51 (1.14) Demographic Age 0.004 (0.34) Education (years) -0.05 (2.18)* Occupational Source of washing water (other = 0, surface = 0.56 (3.47)*** 1) Worked cleaning up an oil spill (no = 0, yes = 0.438 (2.34)** 1) Dietary Number of fish meals / week 0.05 (1.36) Mean Hg in commonly eaten fish -0.37 (0.41) R2 0.13 F value 6.03 P(F) 0.016 Number of observations 75

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01.

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Linear regression models without dietary factors, the sex-appropriate occupational factors (work on spill vs. source of water), education and age while stratifying for sex indicate that the trends are different for women and men (see Tables 5.4 and 5.5). In the case of women, the only significant factor is the source of washing water. Women who use water from a surface source (mean = 3.7 μg/g creatinine, n = 16) have two and a half times the amount of mercury in their urine as women who use water from a well, a spring or the rain (mean = 1.4 μg/g creatinine, n = 14) (see Figure 5.3). For men, the single most significant factor is whether the man was involved in a recent effort to clean up an oil spill. Of the men who had previously worked for an oil company (n = 23), the men who were involved in the operation to physically remove the crude oil on the surface of lagoons had twice as much mercury in their urine (mean = 3.1 μg/g creatinine, n = 6) as did those who held other posts (mean = 1.6 μg/g creatinine, n = 17) (see Figure 5.4). Education was also significant for men – more highly educated men tended to have lower levels of U-Hg.

5.4 Discussion Three key findings emerge from this research. First, the present study shows that some individuals had levels of U-Hg that exceed WHO recommendations despite an absence of exposure to artisanal gold mining or dental amalgams. Second, U- Hg levels in women are significantly associated with the source of the water used for household work. Third, men who were recently employed to clean up an oil spill had double the amount of mercury in their urine as men who were not involved in this effort.

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Table 5.4: Concentration of mercury in urine (log-transformed data) and selected covariates in women: results of linear regression analysis.

Covariate Coefficient (t- ratio) Constant -0.2 (0.18) Demographic factors Age -0.008 (0.42) Education (years) -0.05 (1.06) Occupation1 Source of washing water (other = 0, surface = 0.91 (2.59)** 1) R2 0.23 F value 2.83 P(F) 0.12 Number of observations 30

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01 1 No women were involved in work cleaning up the crude oil spill.

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Table 5.5: Concentration of mercury in urine (log-transformed data) and selected covariates in men: results of linear regression analysis.

Covariate Coefficient (t- ratio) Constant -0.23 (0.6) Demographic factors Age 0.02 (2.03)* Education (years) -0.06 (1.88)* Occupation1 Worked cleaning up an oil spill (no = 0, yes 0.96 (3.34)*** = 1) R2 0.24 F value 4.12 P(F) 0.056 Number of observations 46

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01 1 If location of washing water is included in the model as it was for women, this variable is not significant and the model is qualitatively similar for all other variables.

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5 U-Hg (ug/g creatinine)

0 other Surface water

Source of water for washing

Figure 5.3: Concentration of mercury in urine (μg/g creatinine) of women who use surface water for daily tasks vs. those who use wells, springs or rain water (Corrientes (°), Napo (+), Pastaza (x)). Horizontal line represents grand mean.

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U-Hg (ug/g creatinine) 1

0 Other Spill Clean-up

Employment

Figure 5.4: Mercury concentrations in urine (μg/g creatinine) in men who worked cleaning up an oil spill vs. those who held other positions (Corrientes (°), Napo (+), Pastaza (x)). Horizontal line represents grand mean.

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The upper range of U-Hg in the sample population (15.6 μg/l creatinine) is higher than the WHO limit for unexposed persons (10 μg/l creatinine). Four percent of the population had levels at or exceeding the WHO recommendation of 10 μg/l. Although children were not included in this study, 63% of the population had levels exceeding those which are recommended for children (3 μg/l). Because of children’s increased hand-to-mouth behaviour and time spent in water doing chores and playing, they likely have greater exposure to mercury, in which case their U-Hg levels could be higher than that observed for the study population, making the percentage of children with levels surpassing the WHO recommendations even higher than 63%. Several studies have examined U-Hg levels in persons working in or living near artisanal gold mines, a major source of exposure to inorganic mercury in the Amazon (see Appendix 3). The levels in the present sample population are understandably lower than those found for people working in this industry. The concentration of mercury in the urine of the people living near a mining town are similar to those found in this study population, whereas those living near a smelter are higher (Hurtado et al. 2006). Studies have also reported on U-Hg levels in fish eating populations. The levels found in the present study are similar to those reported in these riparian populations

Previous studies have suggested that part of the inorganic mercury found in urine has its origin in demethylation processes in the body. While U-Hg levels were significantly related to HHg levels in the study population, our data indicate that demethylation of mercury from fish consumption is not a significant source of inorganic mercury for this population. When dietary factors (number of fish meals per week and mean Hg in most commonly consumed fish) are considered alongside occupational factors (working in cleaning up an oil spill and the source of washing water), only the occupational factors are significant. If the mercury in these individual’s urine were coming primarily from fish consumption we would expect to see the number of fish meals and the Hg in commonly consumed fish emerge as significant covariates in the linear regression. It appears that fish consumption is not the source of exposure to inorganic mercury in this population.

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Considering the extent of contamination in the study area and the established link between mercury and petroleum, it is not surprising that the use of local surface water is related to mercury levels in individuals. Women who use water derived from surface sources (the river or streams) were found to have twice as much mercury in their urine as women who sought water from a well, a spring or the rain. The women in the study population spend a substantial part of their time in the water, washing clothes and dishes, bathing themselves and their children and socializing, pointing to partial dermal uptake of Hg. Chapter 6 of this dissertation reports on 1-hydroxypyrene (1-OHP) levels in the present study population and also suggests a partial dermal uptake of PAHs. Research conducted in Korea on volunteers of an oil spill clean-up showed that the wearing of appropriate work clothes, gloves and boots decreased the amount of mercury in urine by roughly half; however, wearing a mask, even a filter mask, made no difference (Lee et al. 2009b). This data suggests that part of the volunteer’s uptake of elemental mercury was via the skin rather than inhalation.

Since this region is devoid of gold mining and hydroelectric dams, the only possible sources of mercury in the surface water are petroleum activities and the leaching of naturally occurring mercury in the soils following deforestation (Mainville et al. 2006). As demonstrated in Chapter 3, deforestation is certainly contributing to mercury levels in the Napo River basin due to the intense rate of land clearing occurring there. As a result of forest conversation taking place on the Ecuadorian side of the Pastaza River, this is a plausible source of some of the mercury observed in these sites. However, there is virtually no deforestation on the banks of the Corrientes River, so it is unlikely that this could be substantially influencing the mercury levels in water from this region. A recent spill upstream from the communities sampled on the Corrientes River is a more likely explanation for the inorganic mercury observed in local residents. Indeed, the community with the highest U-Hg concentrations – Copal – was just a few kilometres downstream from this oil spill and several of the men sampled had

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been involved in cleaning up the damage. Spills are a common occurrence in the region and it could be expected that people’s U-Hg levels would rise and fall according to exposure to inorganic mercury from these episodes. This dissertation also shows that fish from the area around this same spill bioaccumulated more mercury than in other areas (see Chapter 3), indicating that a certain percentage of the methylmercury in individuals is also coming from petroleum activities.

Men who had worked cleaning up this oil spill three to four months prior to sampling were found to have over twice the amount of mercury in their urine as men who were not involved in this remediation. Men described their work in open-ended interviews with the researchers. They recounted how they waded waist deep in ponds dumping an absorbent white powder (Oclansorb) onto the surface. They then collected the crude oil into barrels and burned it. After the bulk of the oil was “eliminated,” their job was to wash the surface of leaves that had been coated with crude oil. This work was carried out with minimal or no protective gear. Of the contaminants examined in the Korean study on volunteer workers (Lee et al. 2009b), only mercury levels were elevated. The authors suggest that this is because the sampling took place when the volunteers were no longer cleaning peak contamination and mercury has a longer half life than other heavy metals and PAHs. Our data on 1-OHP (see Chapter 6) did not display the same trend as our data on Hg; that is, the men who had recently been employed to clean up the spill did not have elevated levels of 1-OHP as compared to those who were not working in this endeavour, most probably for the same reason – the half life of pyrene in the body is a matter of hours to days, whereas the half-life of mercury is months. Local men in the Peruvian and Ecuadorian Amazon are often hired by the oil companies in the event of spills. Just over half of the men in the study population have worked for an oil company. Those who are hired to clean up spills could be expected to be exposed to mercury and other contaminates during their employment.

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5.5 Implications This research highlights the consequences that petroleum exploitation in the Andean Amazon is having on local people’s health. Mercury concentrations in the urine of men who were hired to work temporarily on the remediation of a recent oil spill were elevated as compared to other men. Women using water receiving effluents from the petroleum industry (surface water) were found to have double the amount of mercury as women who used uncontaminated water (well water, spring water or rain water). Concentrations in some individuals exceed levels recommended by the WHO.

Mercury has already been shown to be prevalent in the diet of Amazonian inhabitants due to gold mining, hydroelectric dams and deforestation. This research points to another source of mercury for residents of the Andean Amazon – petroleum exploitation. Workers in this industry should be required to use the appropriate protective gear. Further, it is imperative that the petroleum companies begin re-injecting production water emanating from their activities into the cavity created. In the Peruvian Amazon, protests by local people against the contamination of their environment in 2006 led to a law stipulating that the companies re-inject 100% of their wastes by December 31st, 2007. As of the writing of this chapter the companies have yet to fulfill this obligation. In the Ecuadorian Amazon, ChevronTexaco failed to reinject production waters, line its waste pits or filter burned gas emission and are currently being sued for 16.3 billion $ for negligence by Amazonian locals in the first class-action suit of its kind. The abandoned waste sites need to be cleaned since they are a continuing source of contamination to bodies of water due to seepage and overflowing after heavy rains. More care must be taken to avoid spills. In the event of a spill, crude oil should be removed from the ecosystem since in the sediments it becomes a continual source of contamination to the water.

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Chapter 6: Levels of 1-Hydroxypyrene in Urine of People Living in an Oil Producing Region of the Andean Amazon (Ecuador and Peru)

6.1 Introduction Polycyclic aromatic hydrocarbons (PAHs) are a serious public health concern in urban and industrial areas because of their persistent nature and carcinogenic as well as mutagenic properties. PAHs have also been associated with negative pregnancy outcomes. PAH contamination occurs through direct inputs of petroleum (petrogenic PAHs) or combustion processes (pyrogenic PAHs) (Lake et al. 1979). Heavy crude oil is less volatile than other hydrocarbon mixtures and has a tendency to reside a long time in the environment (NRC 2003). In the first few days after a spill, heavy crude oil loses no more than ten percent of its volume due to evaporation and it is resistant to microbial degradation and photodegradation (NRC 2003). Spills from heavy crude oil are difficult to clean, lead to long-term sediment contamination and have severe impacts on wildlife (Boehm and Page 2007).

Once in aquatic environments PAHs are taken up and accumulated by aquatic organisms (Kochany and Maguire 1994). A study in the Napo River basin of the Ecuadorian Amazon suggests that PAHs emanating from petroleum drilling are bioavailable leading to aquatic toxicity (Wernersson 2004). Studies in other regions corroborate this, showing that PAH levels are elevated in aquatic wildlife near sources of hydrocarbons (Cormier et al. 2000; Fuentes-Rios et al. 2005; Phillips et al. 2006) and oil spills (Salazar-Coria et al. 2007). Bottom-dwelling organisms and benthivores (fish that eat bottom-dwelling organisms) are particularly exposed because PAHs tend to deposit in the sediments (Phillips 1999). PAHs are transferred up the trophic chain, accumulating in top predators of bottom-dwelling organisms (Logan 2007).

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Atmospheric contamination by PAHs occurs through the partial burning of organic material, primarily fossilized material, such as petroleum, natural gas and coal. Heavy crude oil emissions contain more PAHs than other fuels (Yang et al. 1998). Other sources of pyrogenic PAHs are domestic (firewood, incineration, etc.), mobile emissions and agricultural (burning to clear fields, etc.) (Ravindra et al. 2008). Natural sources of pyrogenic PAHs, such as forest fires and volcanic eruptions, are negligible (Wild and Jones 1995). Oil combustion results in a mixture of PAHs containing many of the more volatile PAH species, especially fluorene, fluoranthene, and pyrene (Ravindra et al. 2006)

Pyrene is a four-ring PAH that is found in most mixtures (Buchet et al. 1992). In a study of PAHs in crude oils, which included samples from South America, pyrene was found in 97% of cases (Kerr et al. 2001, p.146). Pyrene itself is not carcinogenic, however many of the other PAHs found in mixtures are. People can be exposed to pyrene through inhalation, cutaneous contact (Boogaard and van Sittert 1994) or ingestion (drinking water (Jacob and Seidel 2002) and food (for a review see Phillips 1999), making environmental monitoring complex. Pyrene absorbed by the body is converted to a metabolite, 1-hydroxypyrene (1-OHP), excreted primarily in urine (Jacob and Seidel 2002) and can be detected at low concentrations (Hansen et al. 2008). Hence, 1-OHP is often used as a bioindicator of recent exposure to mixtures of PAHs through multiple exposure routes (Gallo et al. 2008). Llop et al. (2008) concluded that 1-OHP levels are a good marker of exposure to PAHs in pregnant women.

Many studies have evaluated occupational exposure to pyrene and studies in industrial and urban settings have looked at environmental exposure to atmospheric PAHs (for a review see Hansen et al. 2008). Few studies have evaluated dermal, environmental exposures. A study among people surfing on polluted water indicated that being on the water led to dermal uptake of pyrene and increased excretion of 1-OHP (Jongeneelen 1994). Admissible levels in drinking water have been established for a variety of carcinogenic PAHs in the

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range of 0.03 μg/l to 6.5 μg/l (Rugen et al. 1989, p.273). Few studies have evaluated the levels of PAHs in drinking water (Randow et al. 1996; Li et al. 2006; do Rego and Pereira Netto 2007; Liang et al. 2008; Ma et al. 2008). Orally ingested PAHs are almost completely excreted by three days time (Jacob and Seidel 2002, p.34). The half life when applied dermally is approximately 12 hours (Viau et al. 1995, p.183).

The dominant source of PAHs in non-occupationally exposed individuals is usually through diet, particularly, grilled or charcoaled food; however, foods themselves can contain PAHs prior to cooking (Phillips 1999). Fish, and especially benthic species, living in contaminated water can have high levels of PAHs (Logan 2007). Smoking is an important exposure route to PAHs (IARC 1983). Alcohol consumption has not been shown to affect 1-OHP levels (Van Rooij et al. 1994; van Schooten et al. 1995). Some studies of occupational exposure demonstrate that women excrete more 1–OHP than men (Merlo et al. 1998; Pan et al. 2008); however, most studies find that sex does not influence 1- OHP levels. Women excrete less creatinine, a protein in the urine and used to standardize 1-OHP levels across samples, than men and the creatinine excretion rate decreases with age (Simpson et al. 1978).

Many studies have examined the link between occupational exposure to PAHs and human health outcomes. PAHs are known to cause epithelial cancers such as skin, lung, bronchus and colon cancer (IARC 1983; Phillips 1983). Few studies look at cancer risk and environmental exposure to PAHs (for reviews on leukemia and benzene see Verma and des Tombe (2002) and for cancer and polycyclic aromatic hydrocarbons see Bofetta et al. (1997)). Evidence suggests that co- exposure of carcinogenic PAHs and the sun leads to more potent effects (Shyong et al. 2003; Saladi et al. 2009).

Exposure to PAHs in pregnant women has been associated with negative health outcomes for both the child and mother. Higher levels of PAH-DNA adducts were

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found in foetuses as compared to mothers indicating that these genotoxics might pose a greater risk to the foetus than to adults (Neri et al. 2006). Negative pregnancy outcomes have also been observed. PAHs are associated with impaired pre-implantation embryo development, early embryo mortality, stillbirths, intrauterine growth retardation and reduced neonatal survival (Detmar et al. 2006). A review of articles published on air pollution and adverse pregnancy outcomes in humans determined that there is sufficient evidence to show causality between high levels of air pollution, of which they recognize PAHs as the most important players, and post-neonatal respiratory deaths (Sram et al. 2005). Epidemiological evidence which implicates PAHs in miscarriage rates is also mounting (Sram et al. 2005). A study on mice has discovered the biologic mechanism by which PAHs induce miscarriage of early embryos – induced apoptosis leads to a reduced allocation of cells to the embryo and placenta (Detmar et al. 2006).

Despite strong evidence suggesting the carcinogenic properties of PAHs, the International Agency for Research on Cancer has reported that there is inadequate evidence to state that exposure to crude oil is related to an increased incidence of cancer (IARC 1989). However, epidemiological studies pointing to the carcinogenic outcomes of exposure to crude oil are mounting. Studies in the Ecuadorian Amazon have shown an increased risk ratio for certain cancers in areas contaminated by crude oil in both adults and children (San Sebastian et al. 2001a; Hurtig and San Sebastian 2002a; Hurtig and San Sebastián 2004). Some studies have looked at adverse health effects associated with the sabotage burning of Iraqi oil wells (Osman 1997; Athar et al. 1998). Other health problems associated with crude oil, such as skin problems, have been documented (for a review see Beasley and Burnett 1996).

Few studies have examined pregnancy outcomes in humans environmentally exposed to petroleum products. A study in oil fields of the Ecuadorian Amazon found a significant relationship between contamination and spontaneous abortions

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(San Sebastian et al. 2002). Other studies have found that living near oil refineries is associated with an increased risk of preterm birth (Yang et al. 2004) and low term birth weight (Lin et al. 2001). Studies of pregnancy outcomes in women near petrochemical and coke plants in Sweden, Brazil and the UK, however, did not find an elevated risk of adverse pregnancy outcomes (Bhopal et al. 1994; Bhopal et al. 1999; Oliveira et al. 2002). A study on paternal exposure to oil at work did not show an elevated rate of spontaneous abortions in wives (Bull et al. 1999). Experimental studies of animals exposed to crude oil showed negative effects on bird embryos leading to miscarriage (Hoffman 1979; Lee et al. 1986; Walters et al. 1987).

Jongeneelen (2001) used data on background exposure levels and exposure levels without genotoxic effects to establish a three-tiered benchmark system for 1-OHP. The first level of this benchmark system represents the baseline level. It is the lowest reported level of 1-OHP (for primarily urban populations) and corresponds to 0.24 μmol/mol creatinine for non-smokers and 0.76 μmol/mol creatinine for smokers (p.7). The second level of the benchmark guideline is the no-observed- effect-level and is set at 1.4 μmol/mol creatinine (p.7). Finally, Jongeneelen (2001) proposes occupational levels based on Occupational Exposure Limits (OEL) for PAH concentrations in ambient air. These are 2.3 μmol/mol creatinine for cokeovens and 4.9 μmol/mol creatinine for the aluminum industry (p.9).

The objective of this exploratory study was to report on the levels of 1-OHP in populations living along three rivers exposed to crude oil and wastes from the drilling process. To our knowledge, no studies have reported on the levels of biomarkers of PAHs, such as 1-OHP, in populations of the Andean Amazon living near oil fields. We also make comparisons with the literature reporting on studies carried out elsewhere in the world. Differences in the observed levels of 1- OHP according to geographic, demographic and dietary factors are explored. Finally, the relationship between 1-OHP levels and one important health outcome of exposure to PAHs – miscarriages – is examined.

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6.2 Methods Study Area. The present study was carried out along three white-water rivers of the Andean Amazon (also known as the Upper or Western Amazon): the Corrientes River, Peru, which has been subject to extensive petroleum activity for the past 35 years with an estimated 115,000 barrels extracted per day; the Napo River, Ecuador, which has been undergoing heavy petroleum extraction for the past 45 years and reportedly extracts 500,000 barrels per day; and the Pastaza River, Peru, which has seen petroleum activity in the upper reaches of the study area (Alianza Capahuari) for 35 years and which has just recently signed a prospecting contract in the lower reaches (Loboyacu) (see Figure 1.1). Although there are no marked wet and dry seasons, December to February is relatively drier and May and June are relatively wetter.

Some studies have evaluated the extent of water and sediment contamination by total hydrocarbons in the study area. A study conducted in a village of the Ecuadorian Amazon containing and surrounded by oil wells, found levels of total petroleum hydrocarbons (TPHs) in streams to be 10 to 288 times higher than the limit permitted by the European Community regulations (0.01 ppm) (San Sebastian et al. 2001a, p.520). Levels in streams of the Ecuadorian Amazon used for drinking water ranged from 0.02 to 2.9 ppm (San Sebastian et al. 2002, p.314). Elsewhere in the Ecuadorian Amazon, drinking water was found to have levels of total petroleum hydrocarbons (TPH) above nationally permitted concentrations (Wernersson 2004) and PAHs exceeding the United States Environmental Protection Agency (EPA) recommendations by 10-10,000 times (Hurtig and San Sebastián 2004, p.246). Sediments in the Ecuadorian Amazon were found to have levels of total petroleum hydrocarbons as high as 6980 mg kg−1 dry weight (Wernersson 2004, p.132). A study by the Peruvian government in the Corrientes River found hydrocarbon concentrations in the sediments to be 54.5 mg kg–1 dry weight with some sampling sites as high as 43 595.5 mg kg–1 dw (MEM 1998).

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Another study found levels between 373 and 1 559 mg kg–1 dw (DIGESA 2006, p.19). The maximum permissible concentrations in sediments for a range of PAHs were determined to be between 0.12-10.7 mg kg–1 (Kalf et al. 1997, p.96).

Populations and Recruitment. This study was conducted with people from eight villages along the three rivers (Napo River: Palma Roja, San Carlos, Añangu; Corrientes River: Peruanito, Copal, Nuevo Paraiso, and Pastaza River: Alianza Capahuari and Loboyacu) (see Figure 1.1) in 2006. In the case of all but one of the villages (San Carlos) the nearest city is only accessible by boat. Communities vary in distance from oil wells (San Carlos: 0 km, Loboyacu: 50 km). The participants in this research are primarily Amerindian peoples of the Kichwa, Achuar and Urarina nations. Most people live from subsistence agriculture; however, some people work occasionally for the oil companies and/or the tourism industry. All villages have a primary school, whereas in most villages secondary education is attained through visiting teachers.

The study was explained and permission to work in each community was obtained from the community leader and the community members collectively at a general meeting. Each individual was then visited separately at which point they were invited to participate on a voluntary basis. Interviews took place in a private space in the informant’s home and the sampling was carried out by the individual. The informed consent form was read aloud and participants signed. All adults were eligible and no one incurred reprisal for not participating. No compensation was provided. Ethics approval was obtained from the McGill University Ethics Review Board. Field work was conducted between July and December 2006.

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approximately a half an hour to complete. Since PAHs are known to deposit in the sediments and accumulate in benthivorous fish, diet questions focused on the frequency (number of times per week), species and provenance of fish consumed. Work with petroleum is an important exposure pathway, so the occupational section of the questionnaire focused on work with the oil companies. Women were asked how many miscarriages they had had in their lives. No distinction was made between spontaneous abortions (loss of foetus prior to 28 weeks gestation) and stillbirths (loss after 28 weeks). Questions on cancer were also asked, but few people knew what cancer was.

Since this was conducted as a pilot study, every other person interviewed was invited to provide a urine sample (except when there were more than two people in a household at which point we asked the first person at the next house). Two hundred and twelve people, 15 years of age and older, were invited to join the study by answering a questionnaire. Fourteen people refused. In total, 198 people were interviewed. Of these, 87 were asked to give a urine sample. Four people refused. Six people did not return their urine pot, leaving 77 people who contributed urine samples. Two samples did not contain enough urine after other analyses. The total sample population included 75 individuals. Women from the Urarina community of Nuevo Paraiso did not contribute a urine sample for cultural reasons. Samples were collected as a single void, since the participants were not occupationally exposed at the time of sampling. Samples were kept in a polypropylene bottle (Nalgene™), in the dark at approximately -4-0°C while in the field and then at -20°C until analysis.

Sample analysis. The samples were analysed according to the method designed by Jogneneelen (1987) at the First Nations and Inuit Health Branch Laboratory (FNIHBL), Health Canada in Ottawa. Urine samples were subjected to enzymatic hydrolysis of the conjugated 1-OHP. This was followed by a solid phase extraction and separation by high performance liquid chromatography and fluorescence detection. Lab technicians were blind to the location where each

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sample was taken. The detection limit was 0.1 μg/l. One reagent blank and two calibration standards (Acros Organic_1-Hydroxypyrene) were included every eight samples. Values below 0.1 μg/l (of which there were eight) were entered as 0.05 μg/l. Concentrations of creatinine were used to standardize for diuresis as recommended by Bouchard and Viau (1999). Creatinine analysis was carried out at the Centre de Toxicologie du Québec (CTQ) of the Institut national de santé publique du Québec (INSPQ) using the Jaffe reaction (Microgenics kit #1797) on a Hitachi 917 analyzer. The quantification limit was 0.3 µmol/L (3.3 times the detection limit). Blanks and quality control standards were included in the sequence. The standards were Sigma Creatinine standard Kit part number C361 and QC urine material from MAS Urichem (Thermo), levels L1 and L2. They were included every 10 samples. Values were converted to μmol/mol of creatinine using the equation μmol/mol creatinine = μg/g creatinine * 0.518 according to Hansen et al. (2008).

Statistical Analysis. Descriptive statistics on sex, age, ethnic group, schooling and alcohol and cigarette use are presented. The data for both 1-OHP (μmol/mol creatinine) and creatinine (µmol/l) were skewed (1-OHP: Skewness = 1.4, Kurtosis = 2.2; Creatinine: Skewness = 1.2, Kurtosis = 0.79) so non-parametric tests were used where appropriate; otherwise log 1-OHP concentration was used. The Mann-Whitney U test was used to test for differences between men and women. The Kruskal-Wallis Test of rank sums was used to test for differences in 1-OHP levels between the rivers and communities. A linear regression was run separately for men and women to describe the 1-OHP concentration in the study population. Since the observations were found across villages and observations from the same village tend to share similar unobservable characteristics that could bias usual ordinary least squares estimates, the data was clustered on village (Moulton 1990). The cluster command corrects for such potential intra-class correlation of the errors. A linear regression model was also built to describe number of miscarriages in women. Statistically significant results at p-value of ≤

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0.01, ≤ 0.05 and ≤ 0.1 are shown. Statistical analysis was performed in Jmp 5.0.1a (SAS institute) and STATA 10.0.

6.3 Results

6.3.1 Hydrocarbon Pre-health Outcome: 1-OHP Levels in the Study Population Key socio-demographic characteristics of the study population are displayed in Table 6.1. The median value of 1-OHP for the entire sample population was 0.29 μmol/mol creatinine, the mean was 0.4 μmol/mol creatinine and the range was 0.026-1.62 μmol/mol creatinine. Forty six of the individuals who contributed a urine sample were men (61%) and 29 were women (39%). We did not observe a significant difference in the levels of 1–OHP between men (mean 1-OHP = 0.42 μmol/mol creatinine) and women (mean 1-OHP = 0.37 μmol/mol creatinine) (Mann-Whitney, P = 0.77). Our results also show no significant difference in levels of creatinine between men and women (Mann-Whitney, P = 0.74) (mean creatininemen = 6.19 μmol/l; mean creatininewomen = 5.85 μmol/l). Nonetheless, due to important differences in daily activities, leading to differences in exposure, we stratified for sex. Our results show no significant difference in creatinine with age (ANOVA, P = 0.54).

Smoking is an important exposure pathway for PAHs. One person in the sample population was a smoker (see Table 6.1). This person had a higher 1-OHP level (1.29 μmol/mol creatinine) than the non-smokers (mean 1-OHP = 0.41 μmol/mol creatinine) and the occasional smokers (mean 1-OHP = 0.37 μmol/mol creatinine); but there was no significant difference between the non-smokers and the occasional smokers. There is no significant difference between non-smokers and occasional smokers even when the smoker is excluded (Mann-Whitney, P = 0.22). People in the communities have little access to cigarettes and occasional smoking usually means that they smoke when cigarettes are available, approximately once a month in some villages and once a week in others. Occasional smokers were considered non-smokers for the rest of the analysis.

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Some of the people in the sample population are exposed to pyrene occupationally through their work with the petroleum companies. However, this work is conducted for periods of weeks at a time at which point they are absent from the village where the sampling took place. Hence, we have not captured occupational exposure in this study. The person who had most recently worked for the petroleum companies, returned from his shift several days prior. There is no correlation between the concentration of 1-OHP and the length of time since petroleum workers were last on shift (months) (Pearson correlation coefficient = 0.006, P = 0.98).

No significant differences in the levels of 1-OHP across the different river basins or communities were noted (see Figure 6.2 and Table 6.2). Neither were there significant differences in the levels of creatinine across the river basins and communities (see Table 6.2). The most frequent source of drinking water (river vs. non-river (including: well, spring, stream, rain water)) does vary significantly between communities (Chi Square p < 0.001) and river basins (Chi Square p = 0.02) (see Table 6.2). People on the Pastaza River were more prone to take their drinking water from the river than people on either the Corrientes River or the Napo River. Bathing and washing of clothes and dishes also occurs in different locations according to where one lives (Chi Square p = 0.002) (see Table 6.2). Important differences exist in the species of fish most commonly consumed by both trophic level (herbivore, omnivore and piscivore; Chi Square p < 0.001) and habitat (bottom dwelling vs. pelagic; Chi Square p < 0.001) in the communities and rivers studied here (see Table 6.2).

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Table 6.1: Characteristics of the study population by river and sex in the Andean Amazon: age, ethnic group, schooling, alcohol use and smoking status.

Corrientes Napo Pastaza Characteristic Women Men Women Men Women Men N % N % N % N % N % N % Age 15-24 yrs 3 38 3 19 2 13 1 7 3 60 1 8 25-34 yrs 3 38 6 38 8 50 6 43 1 20 5 39 35-44 yrs 1 13 3 19 4 25 1 7 1 20 4 31 45-54 yrs 1 13 3 19 2 13 3 21 0 0 2 15 ≥55 yrs 0 0 1 6 0 0 3 21 0 0 1 8 Ethnic Group Achuar 7 88 6 32 0 0 0 0 0 0 0 0 Kichwa 0 0 1 5 16 100 14 100 5 100 13 100 Mestizo 1 13 3 16 0 0 0 0 0 0 0 0 Urarina 0 0 9 47 0 0 0 0 0 0 0 0 Schooling None 3 38 8 44 0 0 0 0 1 33 2 17 ≤ 6 yrs 5 63 2 11 8 57 7 58 2 67 6 50 ≥ 7 yrs 0 0 8 44 6 43 5 42 0 0 4 33 Alcohol user 8 100 18 95 14 88 13 93 3 50 9 69 Smoker* 0 0 1 5 0 0 0 0 0 0 0 0

Notes: *Many of the men smoke when cigarettes are available, perhaps once a month.

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Figure 6.2: 1-OHP concentrations (μmol/mol creatinine) by river basin and community. Horizontal line represents grand mean.

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Table 6.2: Mean 1-OHP concentration, source of water, commonly eaten fish and number of miscarriages in the study population River Mean 1- Mean Approx. River as most Surface Bottom Mean Community OHP creatinine distance common water as dweller as number of (μmol/mol (µmol/l) to oil source of most most miscarriages creatinine) (SD) well (km) drinking common common (n) (SD) water (%) washing fish (%) place (%) Corrientes 0.49 (0.33) 5.1 (3.5) 37.0 88.9 81.5 1.8±1.4 (5) Peruanito 0.47 (0.31) 4.4 (2.3) 5 0.0 100.0 70.0 0.5±0.7 (2) Copal 0.42 (0.35) 4.6 (2.7) 20 12.5 62.5 87.5 2.7±1.2 (3) Nuevo Paraiso 0.59 (0.34) 6.3 (4.9) 50 100.0 100.0 88.9 Not applicable Napo 0.31 (0.23) 6.7 (4.9) 16.7 46.7 72.0 0.6±0.8 (16) Palma Roja 0.35 (0.33) 6.9 (5.8) 15 28.6 28.6 71.4 0.7±0.6 (3) San Carlos 0.37 (0.23) 6.7 (3.8) 0 22.2 22.2 75.0 0.5±0.8 (4) Añangu 0.24 (0.16) 6.5 (5.4) 32 7.1 71.4 70.0 0.8±1 (9) Pastaza 0.41 (0.41) 5.9 (5.0) 52.6 52.6 15.8 0.5±0.5 (6) Alianza 0.23 (0.19) 8.5 (5.9) 10 0.0 0.0 11.1 0.5±0.7 (2) Capahuari Loboyacu 0.56 (0.5) 3.8 (3.2) 100 100.0 100.0 20.0 0.5±0.6 (4)

Note: Mean 1-OHP concentration (μmol/mol creatinine), mean creatinine (µmol/l), approximate distance of community from oil wells (km), river as most common source of drinking water (%), surface water as most common source of washing water (%), habitat of fish most commonly eaten (%) and mean number of miscarriages in the three rivers and eight communities.

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A linear regression model was specified using log 1-OHP as the dependant variable and demographic and dietary factors as covariates. The model was run separately for men and women and was clustered on community because several of the covariates were highly correlated with community (number of fish meals and education). Ethnicity is so highly correlated with community that it was dropped from the model. The following were entered as model effects: age, education, number of fish meals per week, habitat of most commonly fish eaten (bottom dweller vs. pelagic), and source of washing water (surface vs. other). For women, where they get their washing water is significant (see Table 6.3). Women who use water from the river or a stream have just under twice as much 1-OHP in their urine (mean 1-OHP = 0.41 μmol/mol creatinine, n = 23) as women who get their water from either a well, a spring or rain water (mean 1-OHP = 0.22 μmol/mol creatinine, n = 6). The source of drinking water also stands out as significant in a linear regression model when it replaces source of washing water. In fact, in all cases, women who take water from the surface (vs. other) or river (vs. other) have roughly twice as much 1-OHP in their urine (see Table 6.4). Education was also significant (p = 0.1) in the linear regression model. The relationship is negative, so more educated women had less 1-OHP in their urine.

For men, the habitat of fish most commonly consumed is the only statistically significant variable (see Table 6.5). Men who reported eating a bottom-dweller as their most commonly consumed fish (mean 1-OHP = 0.50 μmol/mol creatinine, n = 31) had twice as much 1-OHP in their urine as men who reported a pelagic fish (mean 1-OHP = 0.25 μmol/mol creatinine, n = 15). If the linear regression model is built using drinking water instead of washing water this covariate is still not significant. Source of water (drinking, washing, surface or river) was never a significant variable for men.

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Table 6.3: Levels of 1-OHP (log-transformed data) in urine and covariates in women: results of a clustered linear regression analysis.

Covariate Coefficient (t-ratio) Constant -1.43 (1.2) Demographic factors Age -0.02 (1.43) Education years -0.07 (1.82)* Dietary Number of fish meals / week 0.04 (0.55) Habitat of fish eaten (0=pelagic, 1=bottom-dwelling) 0.06 (0.2) Occupational Location of washing water (0=other, 1=surface) 0.58 (2.33)* R2 0.31 F 8.29 P(F) 0.01 Number of observations 29

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01.

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Table 6.4: 1-OHP concentrations in urine of women using different water sources (River vs. Other or Surface vs. Other) for different tasks.

Task Water River Surface Other source 1-OHP 1-OHP 1-OHP concentration (n) concentration (n) concentration (n) Washing - 0.41 (23) 0.22 (6) Drinking 0.79 (3) - 0.32 (26) Drinking - 0.52 (10) 0.29 (19)

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Table 6.5: Levels of 1-OHP (log-transformed data) in urine and covariates in men: results of a clustered linear regression analysis.

Covariate Coefficient (t-ratio) Constant -2.37 (2.73) Demographic factors1 Age -0.008 (0.84) Education years -0.04 (1.42) Dietary2 Number of fish meals / week 0.07 (1.14) Habitat of fish eaten (0=pelagic, 1=bottom-dwelling) 0.79 (2.73)*** R2 0.133 F 4.18 P(F) 0.048 Number of observations 45

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01. 1 Analysis of a similar model including a variable for smoking, for which there was only one smoker and 44 non-smokers, showed that, as expected, smoking is significant (p(t)≤0.01) and resulted in a model that was qualitatively similar for all other variables. 2 If location of washing water is included in the model as it was for women, this variable is not significant and the model is qualitatively similar for all other variables. 3 Including both the variables smoking and washing water yields an R2 of 0.20.

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6.3.2 Hydrocarbon Health Outcome: Miscarriages in the Women of the Study Population The number of miscarriages experienced by women in the study population ranged from 0 to 4 (mean: 0.85; median: 1) (see Table 6.2). No significant difference was found between the number of miscarriages experienced by women on the three different rivers. A linear regression model was constructed using number of miscarriages as the dependant variable and age and log 1-OHP variables as model effects (see Table 6.6). Ethnicity was not included in the model because in this sample of 26 women all of those on the Napo River and the Pastaza River are Kichwa and all of the respondents on the Corrientes River are Achuar. Education was not included in the model either since the variability in education was limited: the majority of women having completed primary school and no more (6 years). The model shows that there is a significantly positive relationship between the concentration of 1-OHP and the number of miscarriages, so the higher the 1-OHP concentration, the more miscarriages the woman reported. Also, older women reported significantly more miscarriages.

6.4 Discussion Four key findings emerge from this study. First, levels of 1-OHP are higher in this rural population exposed to wastes and spills form the petroleum industry than in most urban populations and populations living near industrial activities elsewhere in the world. Second, 1-OHP concentrations in women are associated with using water from the river. Third, 1-OHP concentrations in men are associated with eating bottom-dwelling fish species most frequently. Fourth, the number of miscarriages reported by women participants in this oil producing region is positively related with 1-OHP concentrations.

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Table 6.6: Number of miscarriages and covariates in women: results of a linear regression analysis.

Covariate Coefficient (t-ratio) Constant 0.57 (0.40) Demographic factors Age 0.03 (1.52)* Contamination 1-OHP concentration 0.56 (2.34)** R2 0.22 F 3.18 P(F) 0.06 Number of observations 26

Notes: t ratios are in absolute values * p(t)≤0.10. ** p(t)≤0.05. *** p(t)≤0.01.

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The 1-OHP concentrations found in this rural population (median = 0.29 μmol/mol creatinine, mean = 0.4 μmol/mol creatinine, range = 0.026-1.62 μmol/mol creatinine) exceed the baseline level (0.24 μmol/mol creatinine) set by Jongeneelen (2001, p.7), which was based largely on studies in urban areas. Further, the upper range of the study population exceeds the no-observed-effect- level (1.4 μmol/mol creatinine) also set by Jongeneelen (p.7). Levin (1995) gives background urinary 1-OHP levels for non-smokers in various countries, ranging from 0.03 μmol/mol creatinine (Sweden) to 0.68 μmol/mol creatinine (China) (p.167). Huang et al. (2004) report on non-smoking, non-occupationally exposed controls used in previous studies. The range of median or mean 1-OHP levels from these control populations is 0.02-0.68 μmol/mol creatinine (p.495). Germany has established an official reference value for 1-OHP at 0.155 μmol/mol creatinine (Wilhelm et al. 2008). The mean and median of the current study population are higher than most of the reference values so far reported in the literature and, more importantly, some individuals in the study population have levels exceeding the no-observed-effect-level.

The mean found among this study population exceeds all those found in studies of adults conducted in urban areas, where exposure to atmospheric PAHs released from traffic would be higher than in the study area (see Appendix 4). The values found in the current study exceed even those conducted among smokers in urban areas. People environmentally exposed to industrial activity also tended to have lower 1-OHP concentrations than the current study population. The only studies in which the upper range exceeds that found in the current study were conducted among children who have been shown to have higher levels than adults due to hand-mouth behaviour exposing them to soils (van Wijnen et al. 1996; Fiala et al. 2001). It should be pointed out that there were no children in the present study population. 1-OHP concentrations in situations where indoor air quality is suspected as a major source have also been measured in the literature. Some populations that use wood for household fuel have very high levels of 1-OHP (Viau et al. 2000; Torres-Dosal et al. 2008). The only study that evaluated dermal

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exposure to river water, among wind surfers on the Rhine in the Netherlands, found that people had increased 1-OHP levels on surfing days (0.32 μmol/mol creatinine vs. 0.11 μmol/mol creatinine) (Jongeneelen 1994). Occupational exposures tend to be higher (the highest values have been found in workers in the petrochemical industry: 125 μmol/mol creatinine) (Hansen et al. 2008, p.474). One recent study has looked at offshore oil production workers and found a mean post-shift 1-OHP concentration of 0.15 μmol/mol creatinine in tank operators (Hopf et al. 2009, p.3). It is very telling that the upper range of the study population (1.6 μmol/mol creatinine) is higher than the upper range in most of the environmental studies, except in children in a few of the industrially polluted areas and in the two wood burning studies. Without exposure to urban or other industrial sources, the wastes and spills from the oil drilling activities are the only major source of PAHs in this population.

There was no significant difference in the levels of 1-OHP between men and women in the study population; however, the linear regression analysis indicated that different factors influence the levels observed in men and women. Our results show that women who use primarily surface water (rivers and streams), which receive effluents and spills from the petroleum industry, for their washing have higher levels of 1-OHP than women who get their washing water from wells, springs or rain water. Washing clothes and dishes is a task specific to women while the family is at the homestead. Hurtig and San Sebastián (2004) explain that their results, which show a higher rate of leukemia in girls than boys in areas near oil fields in the Ecuadorian Amazon, could be attributable to a gender-based division of labour.

Fetching drinking water is a chore particular to women and girls. Cooking, which in this study population implies boiling fish, manioc and plantain, is also a task that is performed exclusively by females while families are at home. Previous studies have noted that women’s role as cook places them in contact with PAHs (He et al. 1991; Mumford et al. 1993; Chen et al. 2007). The relationship between

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1-OHP levels and source of water is complicated by the fact that residents in the area know that the water is polluted. This is evidenced by the fact that fewer women (n=10) fetch their drinking water from surface sources than women who use surface water to wash (n=23) and fewer still seek drinking water from the river (n=3). In fact, women who live closer to oil drilling activities are less likely to take water from the river than those who live far away. San Sebastián et al. (2002) also show in their study in the Ecuadorian Amazon that women in exposed communities were less likely to take water from the river. Indeed, in some of the most affected communities, the oil companies have built water wells (Copal, Peruanito and Alianza Capahuari). Hence, a “distance from well” rationale cannot be used to explain the findings because most of the women closer to oil wells use underground water from wells provided by the oil companies. Even so, families regularly go on fishing or hunting expeditions or travel to visit family, in which case they are away from their regular source of water (be it a well, a tank for collecting water or a known spring). On these occasions people more likely than not rely on the water from the river, stream or lagoon (personal observation). The observation that women with higher education have less 1-OHP in their urine could be due to the fact that these women have more knowledge about contamination and are avoiding contaminated sources of water. Indeed, people who get their drinking water from the river had a lower mean education (3.6 years, n = 25) than people who get their water from another source (7 years, n = 50) (Mann-Whitney U, P = 0.0008).

The exposure pattern in men was distinct. Our results show that men who eat more bottom-dwelling fish species have higher levels of 1-OHP. This is consistent with what is known about the behaviour of PAHs in water: PAHs tend to sediment; therefore, fish species that either live in the sediments or eat bottom- dwelling insects, crustaceans and fish have higher levels of PAHs (Phillips 1999; Logan 2007). Our data show that, in turn, men who report eating benthic fish most frequently have higher levels of 1-OHP. Again, the only known source of PAHs to the aquatic environment in the study area is the petroleum industry.

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This study could not control for confounding factors from PAHs emanating from cooking practices; however, the author has reason to believe that the variation in this source would be negligible. Most of the food cooked in the communities is boiled, since cooking oil must be bought, and Zhu and Wang (2003) have shown that boiling food produces the least amount of PAHs. Nonetheless, the study population boils their food over an open fire, so some of their PAH exposure is undoubtedly coming from this route. However, since the use of fire wood is ubiquitous, it does not explain the differences in 1-OHP levels that we found. Few residents have gas stoves, which also release PAHs, albeit less than wood burning (Raiyani et al. 1993), but it is not known to what extent they are used as a substitute for fires since gas costs money and is only available in town. A study in China found no significant difference in 1-OHP levels in non-occupationally exposed subjects who used coal and wood to cook versus gas (Chen et al. 2007). Other studies have shown no effect of cooking habits or heating facilities inside homes on 1-OHP levels (Hansen 2005). It should be noted also that in the Burundi (Viau et al. 2000) and the Mexico (Torres-Dosal et al. 2008) studies where wood was used as fuel, houses were enclosed as opposed to in the Amazon where they are open. A study on cooking practices and 1-OHP levels in China found that women had higher levels of 1-OHP than men and that this was related to the number of times per week that they cooked (Chen et al. 2007). We do not have data on the number of times per week women cook, but since eating at a restaurant is rarely an option in the study population and since raw food is rarely eaten as a meal, this is not likely to vary markedly. Number of children, which might increase the amount of cooking a mother does, has no effect on the models, perhaps because a woman does not cook more frequently when she has more children, but, rather, makes larger meals.

Other sources of pyrogenic PAHs in the study area are limited to the use of generators, outboard motors and open flares from the oil wells. Few people own a generator or boat with a motor and those who do, use them infrequently due to the

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cost of gas. People in the area do not regularly practice slash and burn agriculture (where fields are burned to clear them) because the area receives too much rain. One of the environmentally hazardous practices employed by the petroleum companies working in the Andean Amazon is the burning of excess gases in open flames, known locally as mecheros (Kimerling 1993). Very little is known about the amount of PAHs released in these flames. A study carried out in Kuwait following the Gulf War, when many oil wells were burned, has shown wide spread contamination of the atmosphere by PAHs (Madany and Raveendran 1992); however, biomonitoring studies on humans in Kuwait during the oil fires have been inconclusive as to the genetic damage caused by exposure to open flares (Darcey et al. 1992; McDiarmid et al. 1995; Poirier et al. 1998).

Unfortunately, sampling could not be conducted immediately following a spill since the timing of such an event is unpredictable. Since PAHs are volatile and the river flow takes some of the contamination downstream, we are not capturing peak exposure in this study. Due to the exploratory nature of this study the sample size is relatively small. Further complication could come from the fact that local people, and especially those living closer to oil activities, have noticed worrying changes in the fish (see Chapter 4). Fish are visible harbingers of contamination that are especially sensitive to PAHs (Logan 2007). Our data suggests that this perception is affecting fish consumption (see Chapter 4).

In sum, the evidence on 1-OHP levels in this study population points to multiple exposure routes to pyrene: ingestion of contaminated drinking water and fish associated with contaminated sediments; inhalation of pyrene from wood smoke, oil flares, exhaust from generators and boat motors; and dermal uptake from contaminated sediments. This last source is hypothesized to be the reason we see differences in the linear regression for men and women. While at home, family members usually eat from the same pot, so why is the relationship between log 1- OHP concentration and consuming bottom dwellers only significant for men? It could be because using water from surface bodies of water eclipses the

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relationship in women; however, when both source of drinking water and place of washing are removed from the linear regression model, consumption of bottom dwelling fish does not become significant for women (P = 0.66). Men may eat more fish than women. Our data do not indicate that men eat more fish meals per week than women but it is widely accepted that men eat larger portions. Men could also eat different sections of the fish. PAHs accumulate in the lipid-rich tissues and have been found to be highest in the liver and the muscle (Logan 2007). It could also be that men eat different fish species, portion sizes or parts of the fish while they are on fishing expeditions. Yet, it has been observed that some women also eat differently while their husbands are away, preferentially fishing with a throw net in shallow water and therefore catching bottom-dwelling fish. Men did report eating benthic fish in a greater number of cases (n = 31, 67%) than women (n = 17, 57%), however this difference is not significant (Chi Square P = 0.44). We hypothesize that part of the difference in the significance of variables in determining 1-OHP levels in men and women lies in the fact that men, who are primarily responsible for fishing, are directly in contact with the contaminated sediments while fishing bottom-dwelling fish species, either through standing in the sediments to lay and retrieve nets or in handling the fish once they have been caught. Similarly, we hypothesize that a substantial part of women’s exposure to PAHs is coming from dermal uptake, as well, while they stand in the sediments of the river to collect water, wash clothes and dishes, bathe themselves and their children, and socialize. In any scenario, the levels found in the study population are cause for concern and merit further investigation.

One of the health outcomes associated with exposure to PAHs is negative pregnancy outcomes (Sram et al. 2005). The results reported on above show that people are exposed to PAHs through their daily contact with water. The finding that the number of miscarriages a woman reports is positively associated with log 1-OHP levels indicates that exposure to PAHs in this rural population could be resulting in negative pregnancy outcomes among the women, who spend so much of their time working with water. Age is also an important determinant of

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pregnancy outcomes and it was to be expected that older women would have reported more miscarriages, as they would have also had more pregnancies and the risk of miscarriage increases with age. Our methodology would have probably missed some miscarriages due to recall error or because some miscarriages might have been perceived as delayed menstruation; however, there is no reason to believe that this would be a systematic bias. The finding that number of miscarriages is significantly related to log 1-OHP in women is consistent with what is reported in the literature and is cause for concern. Miscarriages later in pregnancy, in this remote population without access to health care, could have significant consequences on the health of the woman and could even result in death.

6.5 Implications The levels of 1-OHP in the study population are higher than expected in a rural population. Considering that the two main exposure routes to PAHs discovered in this study – water and fish – are an integral part of people’s lives, the results raise concern over the unregimented nature of current petroleum extraction and the growth of this industry in the study area. Our results suggest that the level of 1- OHP found in the study population is having an impact on the number of miscarriages that women are experiencing. Little is known about the consequences of lifetime exposure to PAHs, beginning in the womb and transecting all of life’s stages, but this study implicates petroleum effluents and spills in negative pregnancy outcomes. Further, PAHs are not the only contaminants released by the extraction of petroleum. Heavy metals are also part of the mixture. Some studies have indicated that there are synergies between PAHs and arsenic and lead (Evans et al. 2004; Fischer et al. 2005; Mielzynska et al. 2006). The study population is known to have high levels of mercury (see Chapter 4 and 5), as well as cadmium and lead (DIGESA 2006) also emanating from the petroleum activity in the area. Finally, children, who spend long periods of time in streams and the river to play, cool off, and carry out chores such as washing dishes and fetching water (personal observation), may be exposed to a

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greater extent than adults, especially since they display accentuated hand-to- mouth behaviour, which would lead them to both dermal and oral exposure (van Wijnen et al. 1996; Fiala et al. 2001).

Since PAHs are highly toxic, we recommend that the oil companies in the Andean Amazon cease disposing of production waters into rivers, streams and open pits. Production waters should be reinjected, as is required by law in most countries. Since PAHs adsorb well to soil and sediments (Srogi 2007) and the aquatic environment will remain contaminated for some time, we recommend that the petroleum companies provide wells to all communities that are impacted by oil contamination, including communities located at a distance from oil operations. In the meantime rain water and springs should be prioritized as main sources of water. Proper protective gear should be worn while working for the petroleum companies and while fishing in contaminated sediments. Caution must be taken as to where gardens are placed since soils contaminated in PAHs can lead to the contamination of food crops grown on them (Kipopoulou et al. 1999).

Since our evidence suggests that local people are exposed to pyrene through water, bottom-dwelling fish and sediments, a thorough study of PAH contamination in water and the sediments of these three rivers would be an important step in characterizing the contamination. Sediments are a powerful indicator of environmental contamination since they essentially function as a contaminant trap (Srogi 2007). PAH fingerprinting could be done to definitively identify the source. Further, a larger-scale epidemiological study on the incidence of miscarriages in this population is needed. Considering that the source of contamination in the region - oil extraction - shows no signs of lessening; considering, also, the carcinogenic properties of and the negative pregnancy outcomes associated with PAHs; and considering, finally, the local people’s intimate relationship with their environment, especially the aquatic ecosystem, contamination of the Andean Amazon by PAHs should be considered a major public health concern.

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Chapter 7: Participatory Research and Dissemination of Research Results: The Use of Theatre and Videography

7.1 Introduction

7.1.1 Performance Arts in Health Research The use of performance arts as a recognized means of research and research dissemination has only emerged in the past few decades (Rossiter et al. 2008b). Theatre is particularly well suited to health research because health is an inherently emotive topic. Performance techniques can be employed to garner support for research activities, for example, in enlisting the participation of marginalized and low-income groups who traditionally have low voluntary participation rates (Fritsch et al. 2006). Drama can also be used in the research methodology: to elicit responses from participants or to gather data on personal perceptions. For example, Sinding et al. (2006) used a play, Ladies in Waiting? Life after breast cancer, to collect emotional responses from the audience. Through this methodology they learned the chronic aspects of breast cancer are a major concern for survivors. Another area in which performance arts can be useful is in the validation of data. After an interdisciplinary study carried out using a rapid ethnographic assessment to gather information on the prevalence of strokes, the risk factors, and lay understandings of stroke, Stuttaford et al. (2006) brought their research findings back to the participants in the form of a play to verify that the findings represented an authentic reading of the participant’s initial contribution. Plays have also been enlisted as a pedagogical tool in the training and education of health care professionals, especially to increase understanding of suffering (Kontos and Naglie 2007). Finally, theatre has been most widely used to transmit research results to participants, health care workers and a larger audience (Colantonio et al. 2008; Mason 2008; Rossiter et al. 2008b).

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Theatre and the ecosystem approaches to health are well matched for several reasons. The ecosystem approaches to health promotes methodologies that actively involve participants. Plays – whether they are intentionally interactive or not – are designed to emotionally engage the audience. Participation of community members in the design or enactment of theatrical interventions further enhances appropriation of the material. Combining health research with the arts is also inherently transdisciplinary (Rossiter et al. 2008a). Linking these two disciplines adds new dimensions to research and dissemination, generating novel types of knowledge and attaining a wider audience (Rossiter et al. 2008a). Finally, in the action-research methodology proposed by the ecosystem approaches to health one of the crucial stages of the research is the dissemination of new knowledge and interventions to improve health (Forget and Lebel 2001). Since health data are inherently personal and often highly charged, there is an ethical responsibility on the part of the health researcher to return the results to participants. Returning the results of research is also a way of building enduring relationships based on trust between researcher and participant.

Rossiter et al. (2008b) have classified the use of performance arts in health research into four categories: (1) non-theatrical performances (e.g., monologues); (2) ethnodramas, which use data from interviews, focus groups, etc. to make vignettes; (3) theatrical research-based performances; and, (4) fictional theatrical performances. The third category, theatrical research-based performances, has also been referred to as “improvised ethnodrama” and “ethnotheatre” (Rossiter et al. 2008b). These plays represent the research data or the researcher’s interpretation of the data but do not attempt to faithfully reproduce participants’ interventions verbatim.

Despite the fact that the use of theatre is particularly fitting when communicating research results to illiterate people, examples of its use in low and middle income countries (LMICs) are sparse. In their review, “Theatre as a tool for analysis and knowledge transfer in health research,” Rossiter et al. (2008b) cite only three

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activities that took place in developing countries. The majority were creations for developed world audiences about industrial world diseases: cancer, dementia, Alzheimer's disease, to name a few. In fact, the majority of the theatrical pieces were aimed at health care professionals and medical students, either as pedagogical tools or to disseminate research results. It could be that the literature on this burgeoning subject has not yet captured the wealth of examples coming out of the developing world.

The role of drama as an agent of social change in the developing world has been well documented. While these approaches are similar, the use of drama for social change does not attempt to transfer knowledge about specific research results. For example, street theatre has been used to address issues related to HIV/AIDS in Guatemala and South Africa (Skinner et al. 1991; Savdié and Chetley 2009). Television has been used as a means for health and social justice messaging in developing countries such as Nicaragua (Howe 2008). Dynamic role-playing games have also been developed for social change or to increase understanding between stakeholders. An innovative computer game with three acts helps local people understand the issues at stake in slash and burn agriculture and fertilization in Latin America (García-Barrios et al. 2008).

7.1.2 Multiple Contaminants: An Environmental Health Issue of Importance in the Andean Amazon The rates of deforestation in the Andean Amazon are among the highest in the world. Soil erosion, provoked by deforestation, leads to the leaching of naturally occurring mercury (Hg) into aquatic environments (Roulet et al. 2000; Mainville et al. 2006). Epidemiological studies have associated fish consumption and mercury levels in human populations and correlated decreased motor and sensory capacities with increased mercury concentrations (for a review see Passos and Mergler 2009). However, fish provide a free, high quality source of protein, energy and micronutrients unparalleled by many crops (Tontisirin et al. 2002) and can go far in meeting food security and nutritional diversity needs (Wahlqvist

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2005), an important priority in low and middle income countries. In addition to widespread deforestation, petroleum companies’ activities, which are prevalent in the Andean Amazon, have led to extensive pollution (Kimerling 1993; Wernersson 2004; Martínez et al. 2007). The petroleum industry produces a myriad of toxic chemicals, including Hg, lead (Pb) and polycyclic aromatic hydrocarbons (PAHs) (Phillips et al. 2006). Burning of fossil fuels is a major anthropogenic source of inorganic mercury into the atmosphere (National Research Council 2000). Studies in Kuwait and Spain have shown widespread contamination of the atmosphere and local ecosystems by metals and PAHs due to sabotage burning of oil wells and spills (Sadiq and Mian 1994; Al-Muzaini and Jacob 1996; Gundersen 1996; Perez-Lopez et al. 2006; Al-Hashem et al. 2007). Neurobehavioral effects have been identified as a possible health risk of the open- burning of crude oil at wells (Osman 1997). The nervous system is the main target of Hg and Pb poisoning (Myers et al. 2000; Wright and Baccarelli 2007) and PAHs are known carcinogens (Boffetta et al. 1997). Our earlier research had identified the Andean Amazon as a region at risk of deleterious health consequences from mercury due to volcanic soils laden with mercury (Mainville et al. 2006), high rates of deforestation, regional dependence on petroleum extraction, the reliance on fish as a dietary staple, and mercury levels in fish and human communities (Webb et al. 2004).

7.1.3 Dissemination Strategies and Mercury Research Theatre has not been extensively employed to disseminate the results of mercury research in the studies that have documented their dissemination strategies; yet, other communication methodologies have been documented. In the developed world, strategies to disseminate important information about mercury contamination in fish have revolved around government advisories and media reports (Hood 2005). Much of the attention has been placed on recreational fishers (Burger et al. 2005), hence advisories have been produced by states and provinces on local fish. However, many more people consume store bought fish, which may be from distant markets. Burger et al. (2005) recommend that local governments

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provide information on mercury contamination in the most commonly consumed fish. Other studies have evaluated the efficacy of such advisories. A recent study evaluating knowledge about risks and benefits of fish in a university population found that a lack of detail in the advisories led to confusion among the participants (Burger and Gochfeld 2008). An evaluation of the retention of mercury advisory information in France concluded that messages should be geared toward long-term memorization to be effective (Verger et al. 2007). On the other hand, Oken et al. (2003) found that a cohort of pregnant women had decreased their consumption of certain fish species following a US federal advisory.

Sinikovic et al. (2009) recently found that pregnant women in Australia had little information about the levels of mercury in fish and conclude that a greater effort should be made to transfer data from researchers to health care providers and pregnant women. Holcer and Vitale (2009) describe and evaluate their recent public health campaign disseminating information about mercury risks in Croatia, where there are no government regulations on mercury levels. Educational materials were provided to target groups and the media, and public presentations of hair testing were carried out. The media sustained the topic for 30 days in six TV, two radio and two newspaper transmissions. They conclude that topics on the environmental determinants of health are of low concern to the media and that measures which bring a direct benefit to participants are the most effective. Dissemination of information on mercury in the scientific community has followed tradition, using conferences, journal articles, meetings, and workshops (Pilgrim et al. 2001). Misinformation has been transmitted through the scientific community on occasion. Larsson (1995) found that repeated citations of a misleading scientific paper claiming that dental personnel suffered from reproductive failure as a result of exposure to mercury led to unsubstantiated concerns and erroneous regulations.

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Few of the mercury impact analyses carried out in the developing world have had an educational or participatory component (Hilson et al. 2007); some initiatives, though, have been pioneering. The Caruso Project, spearheaded by researchers at the Université du Québec à Montréal, began in 1994 along the Tapajos River, Brazil, with the aim of evaluating the linkages between human activities and mercury in the environment and human populations, and reducing toxic exposure to mercury (Mertens et al. 2008). The team used a variety of dissemination methods over the years to communicate research results, including workshops, advisories and a comic book. An evaluation of the efficacy of the communication strategy showed that after the intervention, mercury was a discussion topic among most of the participants (Mertens et al. 2005). As part of their research they have been studying the robustness of mercury discussion networks and have found that the network shows resilience in general but is vulnerable to the removal of one individual who has been particularly involved in this participatory research (Mertens et al. 2008).

Several studies on the effectiveness of awareness raising programmes have been carried out in different regions of the world where mercury is employed in artisanal gold mining. In Ghana, where artisanal gold-mining is an important contributor to mercury contamination and where illegal miners are cast as the villains, researchers have sought to involve miners in the sampling of drinking water in order to educate them about the risks of their trade (Tschakert and Singha 2007). The same research team also used participatory hazard mapping, body health mapping and vision mapping to indentify and communicate contaminated sites, heath impacts and ideal small-scale mining scenarios among stakeholders (Tschakert 2009). The author proposes de-stigmatizing the miners as a way of heightening understanding of the complex issues involved and reducing contamination (Tschakert 2009). Hilson et al. (2007) argue that the Ghanaian government’s attempts at mercury awareness raising have focused on implementing generic technologies; whereas, site specific strategies that engage miners in a dialogue are necessary. The United Nations heads up the Global

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Mercury Project (GMP), a project aimed at promoting knowledge and capacity building among Hg miners in Brazil, Indonesia, Lao People’s Democratic Republic, Sudan, Tanzania, and Zimbabwe (Spiegel and Veiga 2005). The project uses Transportable Demonstration Units housing a mercury testing lab, audio- visuals, a classroom, brochures, personal protective equipment and educational street theatre, and staffed by a technical trainer and a nurse (Spiegel and Veiga 2005).

7.1.4 Caution in Mercury Knowledge Transfer: Lessons Learned from the Inuit and Cree In northern Canada, alarmist government advisories targeting the Inuit and Cree led to a variety of unanticipated nutritional, health and societal problems. The contamination discourse in the Arctic conflicted with a deeply rooted system of health based on country food. A study by Santé Québec found that 62% of Inuit were aware that some foods were contaminated, yet only 14% had changed their eating habits as a result and 55% still believe that country food is healthier than store-bought food (Van Oostdam et al. 2005a, p.223). Regardless, acculturation and warnings about contamination have contributed to a decline in consumption of wild foods (Wheatley 1997) and a nutritional and epidemiologic transition is occurring among Inuit of Canada (Kuhnlein et al. 2004). Substitution of wild foods with market foods, often sugar and carbohydrate-based with low nutritive value, leads to a significant decrease in micronutrients (Kuhnlein et al. 2004). Obesity rates have risen among the Inuit since the 1970s and are associated with increased consumption of market food, sedentary village life and reduced hunting and gathering (Kuhnlein et al. 2004). The mortality rate from heart disease is still low among the Inuit of Nunavik despite high rates of smoking and obesity (Dewailly et al. 2001). This phenomenon has been attributed to a high intake of fatty acids through marine mammals and fish, although levels of fatty acids were higher in the older generations (Dewailly et al. 2001).

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Socioeconomic and livelihood consequences have also resulted from dietary changes. Fifty years ago hunting and gathering composed 100% of Inuit food; it now comprises only a quarter. Modern lifestyles in villages have become sedentary and are predicated on wage labour, leaving fewer opportunities for young men to engage in hunting (Condon et al. 1995). The livelihood changes that have accompanied such a shift are dramatic, with consequences for physical activity, identity, and the availability of quality food. The cost of store bought food is still prohibitively high for some (Van Oostdam et al. 2005a) and a large number of women in Nunavik report lacking food (Duhaime et al. 2002). A review of the literature concluded that changing diets and livelihoods are partly responsible for the increased rates of depression, seasonal affective disorder, anxiety, and suicide found in the Arctic (McGrath-Hanna et al. 2003).

Following the discovery of high levels of mercury in the Inuit community of Salluit in the late 1970s, the Canadian government began a campaign of advisories discouraging people from eating certain species and the media propagated sensationalist messages (Wheatley and Paradis 1995; Furgal et al. 2005). As a result, some individuals discontinued their traditional eating habits and switched to market food; however, limited wage opportunities in this remote village meant that such a decision brought on economic hardship (Furgal et al. 2005). Fear consumed the village and the social mechanisms of sharing broke down (Furgal et al. 2005). The consequences of such a drastic shift reverberate throughout the community and touch the foundation of what it means to be Inuit. The Inuit of Salluit have resumed eating country food after the government invested considerable effort to rectify the miscommunication (Wheatley 1997).

Just the opposite occurred in several other villages of Nunavik where O'Neil et al. (1997) found that health policies excluding traditional ecological knowledge led to “counter-knowledge as a form of resistance.” In other words, Inuit food knowledge was turned into a kind of ‘bio-power’ that rejected contamination warnings and extolled the curative agents of traditional food. The scientists’ claim

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that country meat might be unfit for consumption was regarded as false because it ran contrary to what the Inuit had been taught by their elders. These two examples clearly show that if risk communication does not acknowledge the two nutrition discourses – traditional and scientific – each founded upon normative understandings, it could easily fail and result in panic or cultural aggression.

After the risk communication failures of the 1970s and 1980s more attention has been paid to the nutritional and livelihood consequences of changing diets in the Arctic. Risk assessment has been turned over to the Northern Contaminants Program (NCP), which takes into account the dangers associated with contaminants but also the nutritional, cultural and economic benefits of continuing to eat country foods on a case by case basis using a multidisciplinary team composed of scientists, local government and community members (Van Oostdam et al. 2005a). Innovative solutions to reduce toxic exposure and maximize nutritional intake of country foods have been developed. A pilot project funded by the federal and provincial governments and run by the regional authorities is providing free arctic char to pregnant women in an effort to reduce exposure to methylmercury and increase fatty acid intake (Duhaime et al. 2004). With a nuanced and sensitive approach, health is not at the exclusion of the traditional diet and livelihood of the Inuit.

Mercury contamination and alarmist advisories have also been partly responsible for a general decrease in the consumption of fish among the Cree of James Bay, although the pattern is heterogeneous (Belinsky et al. 1996). A move away from a traditional diet, and the reduction in physical activity that has accompanied it, has been associated with obesity, dental caries, anaemia, immune suppression and diabetes (Thouez et al. 1989). In northern Québec Cree communities, diabetes prevalence jumped fourfold between 1989 and 2001, and currently the age- adjusted prevalence is nearly 15%, three times the Canadian average (Rock 2003, p.136). Prevalence increases with decreasing latitude, a proxy for access to market food (Brassard et al. 1993). Inland prevalence was twice as high as coastal

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prevalence, where people rely to a greater extent on wild foods. Environmental risk factors include high body mass and a lack of physical activity, both characteristic of the dietary shift taking place among the Cree (Young et al. 2000; Rock 2003). The Cree attribute the diabetes epidemic to “the decline of bush life” (Rock 2003). Diabetes causes microvascular disease (diabetic nephropathy or retinopathy) (Brassard and Robinson 1995) and problems for the cardiovascular system, immune system, eyes, kidneys and nerves, resulting, at times, in premature death or disability (Young et al. 2000). The increasing prevalence of diabetes has been cited as one of the main factors influencing a recent increase in heart disease in this population (Brassard et al. 1993), but a study by Dewailly and colleagues (2002) found that a traditional diet high in fish fatty acids protects against heart disease in the James Bay Cree.

The unemployment rate in Cree territory is one and a half times greater than in the rest of Québec, and full-time, year round work is also less common (Willows et al. 2005). One fifth of Cree women interviewed expressed anxiety over not having enough money to buy food for their babies (Willows et al. 2005, p.56). A study looking at factors related to mental distress found that spending less time in the bush in the previous year significantly impacted Cree subject’s sense of well- being (Kirmayer et al. 2000). Finally, the lived experience of diabetes has broad consequences, often contributing to the duress that initiated poor eating habits (Rock 2003).

The political climate in which dramatic food warnings arose is evolving. In an attempt to redress some of the problems that arose in Cree communities, the James Bay and Northern Quebec Agreement (JBNQA), signed by Quebec, the Cree and the Inuit in 1975, stipulates that impact assessments be conducted in collaboration with Cree and Inuit, explicitly for the protection of traditional livelihoods (Peters 1999). The agreement provides monetary compensation to those hunters whose trap lines were inundated and whose fish were contaminated and also provides a salary for families who spend a certain number of days on the

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land to encourage traditional land use (Kirmayer et al. 2000). In the case of the Cree, the diet trade-off protecting against methylmercury intoxication came at the expense of health, nutrition and wellbeing. Fish advisories that avoid generalities and are explicit about contaminated species and sites can help curtail the loss of livelihood and the deterioration of diets and health in James Bay territory (Wormworth 1995; Girard et al. 1996).

This chapter describes a dissemination activity that took place in the Ecuadorian and Peruvian Amazon and that used as its main means of communication an interactive theatrical research-based performance to describe research results from a study on mercury and PAH levels in the area. We describe measures taken to avoid the negative consequences that mercury advisories have had in the Canadian North. In the Discussion and Conclusions we reflect on some of the advantages and disadvantages of this approach and suggest ways in which the efficacy of the activity could have been evaluated.

7.2 Methods The activity described here was devised as a communication strategy to disseminate the results of our research project on deforestation, petroleum contamination and exposure to heavy metals and polycyclic aromatic hydrocarbons in riverside communities of the Andean Amazon. To achieve this, we combined diverse expertise and capitalised on networks to build an interdisciplinary, intervention-oriented strategy. Our team consisted of Dr. Quizhpe, an Ecuadorian medical doctor working in the Amazon; Mr. Mauricio Delfin, a Peruvian film maker; Mr. Nicolas Mainville, a biologist; and Mrs. Jena Webb, author, principal researcher and doctoral candidate (Department of Geography, McGill University).

In our research, we determined the levels of mercury in human hair (n = 192) and local fish (n = 486) species and PAHs and inorganic mercury in human urine (n = 76) in three biogeochemically similar rivers with differing land-use

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characteristics: the Napo River (Ecuador), the Pastaza River (Peru), and the Corrientes River (Peru). We used regression techniques to examine the associations between the levels of contamination and socio-demographic, occupational and dietary factors. Our research demonstrated that levels of mercury in some fish species and community members were above the WHO limit for safety. Water was also found to be an important exposure pathway for women. Local people needed to be made aware of the levels of contaminants in their fisheries so that they could make informed decisions that would minimize potential harm of fish consumption, while at the same time encouraging consumption of untainted fish. Policy makers, the private sector and health practitioners also needed to be appraised of the contaminant risk in order to adjust their policies and practices. We felt that there needed to be a strong public communication strategy to disseminate the results of the research in order for it to translate into improved population health.

Activity Objectives - Knowledge Exchange and Dissemination Our knowledge exchange and dissemination strategy was devised to address four ‘research to action’ challenges. Our first research to action challenge was to draft an audience appropriate strategy of informing the public, local government and the private sector of our research findings and recommendations. It was crucial that our recommendations be sensitive to the fact that fish are a mainstay for local people. A second research to action challenge constituted how to endorse sustainable agricultural practices among small land holders without overburdening individuals. Our third challenge corresponded to how to influence governments to take into consideration the human health implications of deforestation and petroleum exploitation. Our fourth challenge was how to impress upon the petroleum companies the importance of a clean environment to the health of local people. Finally, all of this needed to be done without precluding dialogue and with an aim to linkages between stakeholders for future research. Our strategy relied on addressing four spheres of influence that play a role in the contamination problem in the Andean Amazon: diet, land use, national

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policies and oil extraction. To speak to each of these spheres we coined four key ‘actionable messages.’

The anticipated outcomes of this activity were:

• a dietary shift towards fish lower on the food chain • no reduction in overall fish consumption • a reduction in mercury levels in the residents of the visited communities • retention of traditional agricultural practices and reduction of deforestation in communities • guidelines that would have an influence on government policy regarding conservation and the practices of petroleum companies • raised awareness of the situation among health practitioners and civil society • definition of research priorities and creation of links with local stakeholders who could contribute to future studies • training and mentoring of two young LMIC researchers (Dr. Quizhpe and Mr. Delfin) • maintenance of a sustainable research environment in the region.

7.2.1 Research to Action Challenge 1 – The Use of Theatre and Video in Knowledge Transfer among Amazonian Riparian Populations The first actionable message, ‘eat more fish that don’t eat other fish,’ (Lebel et al. 1998a) targeted community members. This is a positive statement that recognizes the benefits of fish meat and encourages people to eat more fish, while at the same time steering community members away from highly contaminated predatory fish. The expected outcome was that people eat more fish that do not eat other fish thereby reducing their exposure to contaminants and decreasing health risks.

The core of the work in disseminating this message was done through workshops in five of the communities (Palma Roja, San Carlos and Añangu, Ecuador, and Alianza Capahuari and Loboyacu, Peru) (see Table 7.1). At these workshops the dynamic of mercury and other contaminants was explained using theatre, the parts of oil well, tree, fish, and humans being acted out with costumes by community members themselves. The costumes were made by a local woman in order to capture local aesthetics. The costumes were also simple; this was the first time

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theatre had come to these remote villages and props and costumes that were too elaborate would have been exaggerated and clashed with the setting. We convened the workshops ahead of time and when we arrived in the villages community members were abuzz with excitement and consequently there was a high participation rate at the workshops. The workshops were held at the local communal meeting place. We enlisted a community member to translate parts of the workshop. In San Carlos an additional presentation was made in the elementary school. Mr. Nicolas Mainville and Dr. Edy Quizhpe animated the workshops, beginning by reminding people of the research we had conducted two and a half years prior. We explained that we were back exclusively to return the results of the research in the form of a play to participants and not to conduct further research. We then began the play.

First, the narrators explained the props: black cubes were petroleum and the contamination contained therein, red circles were mercury, and green triangles were nutrients. The nutritive quality of fish was emphasized right from the outset of the play. We set the scene by delimitating an imaginary river in which we placed some branches to represent aquatic plants. We asked for a volunteer to play the part of an oil well. This usually led to laughter and some hesitation. Invariably, a man was coaxed into getting on the “stage” by his fellow community members. We pulled the costume over his head and gave him a bucket filled with petroleum and mercury props. The narrators asked the “oil well” to dump the “pollution” into the river. The narrators reminded the audience what each prop was and explained that mercury fixes to aquatic plants, placing several of the “mercury” on the branches.

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Table 7.1: Location, date and participation at the six performances of our play

Location Date Number of participants (approx) Palma Roja, Ecuador March 13, 2009 40 San Carlos, Ecuador March 17, 2009 20 Elementary school March 17, 2009 20 Añangu, Ecuador March 22, 2009 40 Alianza Capahuari, Peru April 5, 2009 50 Loboyacu, Peru April 6, 2009 35

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Figure 7.1: Mr. Mainville and Dr. Quizhpe helping a community member of Añangu, Ecuador, become an oil well.

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Scene two depicted deforestation. We asked for a second volunteer and had him put on a tree costume. This incited uproarious laughter because the trunk was a brown skirt and the volunteer was again, invariably, a man. A third person was asked to cut down the tree and we often had an enthusiastic volunteer. Because of community dynamics, this scene was very lively, giving one man an opportunity to “cut down” the “tree.” We had placed “mercury” at the feet of the tree and explained how mercury in soils ends up in the river after trees are cut. Again, the mercury ended up in the plants.

Scenes three, four and five illustrated bioaccumulation. We asked the audience which fish species eat plants and had various responses. We asked for a volunteer to be a palometa (Mylossoma duriventre) – a herbivorous fish. The narrators pointed out the green triangles attached to the fish costume with paper clips and commented on the high nutritive quality of palometa. The narrators asked the palometa to eat the plants and explained that when the palometa eats the plants it also ingests the mercury, so the narrators handed the palometa several red circles, which the fish kept in his hands visible to the audience. A volunteer was enlisted to be a small piscivorous fish, fasaco (Peruvian name, guanchiche in Ecuador) (Hoplias malabaricus). The “fasaco,” which also had green, nutrient triangles attached to its body, was instructed to eat the palometa. Often an energetic chase ensued. Once the palometa was caught, the narrators explained that the fasaco, in eating the palometa, also ate the mercury. The narrators then asked the fasaco to eat another palometa and explained that it would then ingest even more mercury. A final fish volunteer was asked to play a large piscivore, a bagre (Brachyplatystoma sp), and replicate the same sequence ending up with even more mercury.

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Figure 7.2: Community member cutting down a tree in the play performed in San Carlos, Ecuador. Note mercury props at the “tree’s” feet.

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Figure 7.3: A fish fight between a palometa and a fasaco in Palma Roja, Ecuador. Note triangles representing nutrients hanging off the fish (circled in white).

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Figure 7.4: A bagre in Añangu, Ecuador, with a lot of mercury. Palometa and fasaco in background.

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The penultimate scene involved a fisherman recruited to catch several fish. The mercury was given to him and placed under his shirt. Nutrients pinned to the fish were also given to the fisherman to underscore, once again, the nutritive qualities of fish. More and more mercury was inserted into his shirt as he caught piscivores. The final scene enlisted a woman to fetch water from the “river.” The narrators placed “petroleum” and “mercury” in her cauldron and explained that when we drink or cook with water from the river we are exposed to toxic chemicals.

A game involving children followed the play. The game was Dr. Quizhpe’s idea and initiative. We asked for ten children to come to the front and we gave them each a tee-shirt. The tee-shirts had the parts of plant (4), palometa (3), fasaco (2) and bagre (1) printed on them. We provided each of the “plants” with a couple of mercury props. We asked the kids to chase each other and “eat” that which was appropriate to its species, transferring the mercury each time. At the end of the chase, when the bagre had all the “mercury,” the narrator played the role of fisherman and chased the bagre. After the game we opened up the session for a discussion period. These discussions were often lengthy and consisted of in-depth questions. For example, one participant asked, “If we clear land that is not on the river bank will the mercury get into the river?” Finally, each participant in the study was given their personal results in a letter, making the topic more tangible, and a laminated poster with information on the nutritional value of fish and contamination in fish (usually younger members of a household are literate). A tee-shirt was given to each child in the audience.

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Figure 7.5: A fisherman in Añangu, Ecuador, with a lot of mercury and nutrients in his belly.

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Figure 7.6: A woman from Añangu, Ecuador, fetching water in the river.

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Figure 7.7: Mr. Mainville playing the role of fisherman in the game played in Palma Roja, Ecuador. Note “mercury” (circled) in the hand of the child “bagre.”

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A medium sized documentary for the internet (22 min) was produced by Mr. Delfin while we were disseminating the results in the two Peruvian communities. The video, Zona Cruda, carries the message to a wider audience. Zona Cruda documented the theatre experience, exchanges between researchers and community members, and the peoples’ voices. Mr. Delfin, as director, had artistic discretion and made decisions on the content of the video. As a Peruvian, this ensured that the video had cultural relevancy. We launched the video, sending an email to approximately 500 people. The video is hosted on our blog and in Vimeo (http://vimeo.com/6812936) and has been viewed by over 1,500 people.

7.2.2 Research to Action Challenge 2 – Endorsement of Sustainable Agricultural Practices among Small Land Holders The second slogan, ‘protecting the forest protects your health,’ addressed land use and was geared to communities, NGOs and local and regional governments. The anticipated outcome was that people consider the health consequences of clearing land on river banks and return to or retain traditional shifting cultivation in plots set aback from the river. The message was spread through the theatre, the video, a poster and a technical report. Traditionally, small garden plots were cleared in forests, leaving at least several meters of forest growth between a plot and the river. Nowadays, migrants are practicing cattle ranching and often place pastures directly on the river banks augmenting the amount of mercury that enters the river. Some native farmers are emulating the newcomers and the rate of mercury entering watersheds risks to accelerate as new migrants arrive and long-standing residents change their practices. By engaging elders in our workshops with the communities we hoped to reinforce traditional knowledge and to open up a dialogue about the advantages and disadvantages of agricultural site selection. Our theatrical piece and the video addressed the role of deforestation in the contamination of fisheries by mercury. A poster including information on best agricultural practices was handed out to participants of the workshop. Information was also provided to conservation and agricultural development initiatives

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(governmental and non-governmental) in the form of a 16 page technical report written in Spanish.

7.2.3 Research to Action Challenge 3 – Linking with Policy Makers The third actionable message, ‘world class environmental standards are needed to protect people's health,’ speaks to Peru and Ecuador’s emergence as rapidly developing countries and caters to their desire to be viewed as responsible nations. Increased concerns and pressure from the international community to reduce deforestation, an important contributor to climate change and biodiversity loss, is leading tropical countries like Peru and Ecuador to take concrete actions towards conservation. The expected outcome was that the government would use this health issue to promote conservation in the Amazon and enact changes in the environmental standards applied to petroleum exploitation. This message was directed to the ministries of health, environment, natural resources (mining and energy) and agriculture in each of the countries as well as conservation and health NGOs. We held a strategic meeting with 20 individuals from the ministry of Health (members of the other ministries were invited but did not attend) in which we presented the results of the study. In a previous dissemination campaign in Ecuador we were able to meet with then Minister of the Environment, Mr. Edgar Isch Lopez. Finally, through the documentary and other venues we hope that this message has infiltrated the media (the video was profiled in the Peruvian newspaper, La Primera, (17/02/10)).

7.2.4 Research to Action Challenge 4 – Corporate Responsibility Our fourth line of action aimed to impress upon the petroleum companies the idea that ‘shareholders are increasingly demanding cleaner practices.’ Much of this work has yet to be completed and will form an ongoing effort to make the situation known in Canada through a blog, technical reports, publications, shareholder meetings, the media, ethical investing circuits and meetings with

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NGOs, lawyers and top executives in Canadian oil companies, which have operations in Peru and Ecuador. We have begun this work by creating a blog that we hope will become a respected source of scientific information for scientists and practitioners seeking information on the health impacts of petroleum extraction (www.zonacruda.wordpress.com). We have a section with entries highlighting current events, a reference page and a link to our video. The hope is that these activities will add to a growing global demand for responsible business practices.

7.3 Discussion and Conclusions The use of theatre in knowledge transfer has obvious advantages, many of which were outlined in the introduction of this chapter. Through the experience described here we confirmed several of these presuppositions. Through correct answers to our questions during the performance, pertinent questions and children’s comprehension of the game played after the play, our experience has shown that theatre is an effective way to convey a complex scientific idea and findings, especially with respect to bioaccumulation, a topic that even university students can have difficulty comprehending. The transfer of mercury from source through to humans is an inherently visual affair since it involves movement (as opposed to a subject matter such as cellular division in cancer research) and lent itself well to the chosen medium. We also learnt that, despite our initial fears, people were eager to engage. The recruitment of volunteers as actors in the play was seamless after the initial volunteer broke the ice. Further, the volunteers had no trouble following the instructions given by the narrators. This system heightened the participants’ involvement in information acquisition by directly involving some members of the community or by involving an individual’s family member (since in these tight-knit communities almost everyone is related). Finally, the simple act of returning the results to the research participants in a way that valued their participation, prioritized maximum understanding and took their enjoyment into consideration, contributed to building trust in a region where many local people complain of researchers gathering information that is never

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made available to the people who so laboriously provided it. We have observed that the communities where we returned the most often (five times) are the communities in which we have the most amicable and collaborative relationship. The video was an effective way of broadening the audience, since the number of live performances was limited.

The limitations of this approach include the relatively weak involvement of women, minimal interest on the part of policy makers, and limited funding opportunities. At the end of each performance, we insisted that a woman come up to fetch the water, because this is traditionally a woman’s task. After some probing from her compatriots, we often ended up with a woman who seemed happy to play the role. We could have tried harder to involve more women as actors from the beginning, although we didn’t want to overstep social boundaries either. The same problem arose in making the video. We asked several women to give testimony but none volunteered and we were not inclined to insist. Getting women to speak in women only focus groups led by Mrs. Webb during the data collection was not exceedingly difficult, but engaging them in public activities proved challenging. Traditionally, men occupy public posts (president, vice president, treasurer, etc.) and are more vocal at community meetings. Men tend to speak better Spanish in these Kichwa communities. Unfortunately, our efforts to address policy makers were not very successful. Members from ministries other than the Peruvian Ministry of Health did not attend our presentation and we have witnessed no uptake of the information in the form of policy shifts. Another limitation we had was related to funding. Our budget only allowed us to go to five of the eight communities visited on the original sampling campaign. Without electricity, computers, or projectors in villages, the video we made is not useful to those communities that did not have the opportunity to see the live performance. Lack of funding for dissemination is a chronic problem in academia, which valorizes data collection and knowledge creation more than knowledge transfer and interventions.

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The play that we presented to research participants in Amazonia was very well received, incited laughter and responses to our questions (signs of engagement) and led to a fruitful discussion period. Unfortunately, however, due to time and funding limitations we were not able to formally evaluate the efficacy of the activity. Many participatory approaches integrating theatre have been evaluated, yet a consistent methodology for doing so has yet to be developed (Rossiter et al. 2008b). Three methods have been employed: unstructured forms of feedback (e.g. reflective journals and informal discussions), structured but open-ended questionnaires, and highly structured, quantitative surveys. Because the population is largely illiterate, a written evaluation method such as a journal would not be appropriate for the present activity. But how could the activity have been evaluated?

The first question to address is, “what result would we anticipate from a successful presentation?” Are we hoping that participants enjoyed the performance, that the performance attained a certain level of theatrical excellence, that the members of the audience learned something of the subject matter or that they change their behaviour in accordance with the information presented to them? Further, are we looking for a short-term or a long-term effect? While it was important to us that the audience enjoy our play, this was primarily a means to an end. We hoped that the piece would be engaging enough to effectively convey scientific information to a primarily illiterate population in a way that they could visualize, understand and retain.

Since the anticipated outcomes of the dissemination strategy were a decrease in the amount of mercury in participants’ hair, a reduction in the amount of piscivorous fish consumed, and no net change in the total number of fish meals consumed per week, the evaluation would have to address these issues and be comparable to the data we collected in 2006, before the play. A two-step evaluation is foreseeable. First, hair samples from the individuals who provided samples in the initial sampling campaign and who were at the performance could

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be measured for mercury and analysed in a matched pairs analysis with the 2006 results. The optimal evaluation method of fish consumption would be a highly structured quantitative survey with open ended questions. Two quantitative questions similar to those on the initial survey would be “What are your most commonly eaten fish?” and “How many fish meals do you eat per week?” These could again be compared to the 2006 results in a matched pairs analysis. Two complimentary open ended questions would be: “Has your consumption of fish changed since the play (x months) and, if so, how?” and “Why have you changed your fish eating habits?” This methodology would be identical to that which was employed in our study on the changes in mercury levels and fish consumption in the community of Añangu following their entry into the ecotourism industry (see Chapter 4). To measure if there were long-term behavioural changes the same evaluation method could be used a year after the performance.

In addition to these indicators, community members could be invited to suggest indicators of importance to them. A brainstorming session could be held after the play to see what changes the community members would like to see and which they would avoid. For example, they might value time fishing and wish to see an indicator that addresses this. They might also raise the issue of cost: nets used to catch herbivores require cord and this type of fishing is practiced in lagoons reached by boats necessitating gas. These indicators could be used in conjunction with the indicators outlined by the researcher. This would be a participatory method for designing an evaluation.

A more comprehensive way of evaluating an intervention is suggested by Forget and Lebel (2001) in their ecosystem approaches to health action-research methodology. If a larger audience including policy makers and oil company executives had been successfully reached this could have been undertaken. They recommend beginning with using the “effect” as an indicator for the efficacy of the intervention. In this case the “effect” would be hair mercury levels. Then we could have measured indicators of “exposure” (fish consumption through a

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questionnaire), the “state of the ecosystem” (mercury levels in fish), “pressures” (petroleum extraction practices and deforestation in the field) and “causes” (changes to environmental standards and verification of existing standards). This methodology is akin to using the anticipated outcomes as benchmarks. The exposure indicator – fish consumption – would allow us to evaluate if the message was misconstrued. If people reported a decrease in the number of total fish meals per week we might learn that the activity had not attained the goal of promoting the consumption of herbivorous fish and rather, led people away from eating fish.

Indigenous groups in the Amazon are often self-sufficient in food and depend entirely on subsistence agriculture, fishing, hunting and gathering for their livelihoods (Dufour 1992). Some authors are of the opinion that, irrespective of the levels of mercury in fish and humans, the health and economic benefits of eating fish greatly outweigh any potential deleterious impacts in the Amazon (Dorea 2003, 2004). It is unlikely that many indigenous groups in the Amazon are changing their livelihoods and limiting their fish intake based on risk of methylmercury exposure since communication in this vast territory is limited and people have few other options (as opposed to the Inuit and Cree who have greater access to market goods); yet Kligerman and colleagues (2001) reported that gold miners on the Tapajós River did not eat fish because they were aware of methylmercury contamination. Studies on the livelihood (Behrens 1989; Stearman 1990; Behrens 1992; Vickers 1993; Behrens et al. 1994) and nutritional changes (Hodge and Dufour 1991; Lindgärde et al. 2004; Godoy et al. 2006a; Godoy et al. 2006b) accompanying modernization in the Amazon indicate that change brings about certain hardships, but none refer specifically to mercury exposure risk management as a driver of change. Since Amazonian diets are considered undersupplied in fat, a departure from fish consumption could be especially detrimental for children who require higher density foods (Milton 1991). In order to avoid the mistakes that were made in northern Canada, warnings about mercury contamination in the Amazon should be approached with care and conducted with the aim of developing solutions, keeping in mind the health and socioeconomic

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consequences of dietary shifts (Webb 2005). This activity repeatedly emphasized the nutritional qualities of fish and used a positive slogan, “eat more fish that don’t eat other fish,” to promote the message. Further, the information given to participants was trophic level and species specific. Local people know very well if a fish species is a herbivore or a piscivore. Our play showed the negative impacts of eating an excessive amount of piscivores and encouraged the consumption of herbivores. Finally, the printed information that was provided to each household, supplied participants with lists of specific fish species that are not contaminated, moderately contaminated and very contaminated.

Participatory research methods are challenging to implement and, thus far, rare. Recent examples of participatory approaches in health research in the Peruvian Amazon include the construction of problem trees in prioritizing health problems in an urban slum (Casapia et al. 2007) and the use of drawings in workshops on evaluating the efficacy of radio broadcasts on gender equity and reproductive health (Singhal and Rattine-Flaherty 2006; Rattine-Flaherty and Singhal 2009). In the Ecuadorian Amazon, a popular epidemiological study on health and oil contamination enlisted local organizations to formulate hypotheses, collaborate during the study and spearhead the dissemination activities (San Sebastian and Hurtig 2005). To our knowledge, no health research systematically using performance arts in the Peruvian and Ecuadorian Amazon have been reported on. Despite its intuitive aptness for communicating research results to primarily illiterate populations, theatre has been underemployed in this domain. The reasons for this may include a lack of commitment to dissemination on the part of researchers and funding agencies, the inherent complexity of working across disciplines and fear. It takes courage and commitment to step out of our comfortable spheres and undertake something radically new. From this experience, though, we highly recommend that researchers go the extra mile to render research results digestible for participants and, if appropriate, to use theatre to do so. In the end, the information belongs to the research participants. The trust and respect gained by so doing are immeasurable and invaluable.

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Chapter 8: Conclusions This dissertation drew upon mixed methods to investigate environmental contamination in the Andean Amazon and its association with the petroleum industry and frontier colonization. The findings suggest that resource development in the study region has significant negative impacts on the health of local people through exposure to toxic chemicals. Poverty has been posited by some as the main underlying driver of deforestation. Economic development is thought to alleviate the pressure that poor people put on tropical forests for survival. Chapter 2 showed that a large body of literature is now challenging this view. Deforestation seems to continue in spite of, and even because of, development and poverty reduction in many cases. Further, the benefits of economic development do not always trickle down to local people. Deforestation has negative consequences on the ecosystem, but also on the health of local people who eat fish that become contaminated with the mercury leached from eroded soils. Petroleum extraction has left a legacy of toxic contamination that contributes to mercury levels and adds new contaminants to the mix. Several indicators were used in this doctoral research to examine the negative consequences associated with the development of the petroleum industry and the colonist deforestation resulting from increased access to markets that the presence of petroleum companies affords. The findings point to water and fisheries contaminated by both mercury and PAHs.

The specific objectives of this dissertation were:

1. To determine the levels of mercury in commonly consumed fish species in the Andean Amazon. 2. To determine the levels of mercury in the hair and urine of rural populations living in socially and geographically contrasting settings of Andean Amazonia and to evaluate the environmental factors, particularly deforestation and oil extraction, contributing to this contamination. 3. To determine the levels of 1-hydroxypyrene in the urine of rural populations living in socially and geographically contrasting settings of Andean Amazonia and to evaluate the role of oil extraction to this contamination.

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4. To examine the incidence of miscarriage in women of the study population in relation to levels of 1-hydroxypyrene. 5. To effectively communicate the results of the research to study participants, national government agencies, health care providers and non- governmental organizations.

The remainder of this chapter is organized into two sections. The first section reviews the findings of each empirical chapter (Chapters 3 to 7), commenting on how the findings respond to the objectives of the study, detailing the substantive and methodological contributions to academia and acknowledging the methodological shortcomings. This section concludes with a comment on the methodological contribution of the overall study design. The second section draws on the key findings from each chapter. These findings are contextualized, cross- cutting elements are highlighted and recommended policy changes are outlined.

8.1 Chapter Summaries Chapter 3 examined mercury levels in fish and the impact of deforestation and petroleum extraction on these levels. Mercury levels were determined in 486 fish samples from 61 species collected in the three river basins. Data was stratified by trophic level. Fifteen percent of piscivores and eight percent of carnivores were found to have levels of mercury above the WHO safety recommendation (0.5 μg/g, wet weight). Piscivores were found to have the highest levels of mercury (mean: 0.28 μg/g) and herbivores the lowest (mean: 0.04 μg/g). One particular species, Hoplias malabaricus, was investigated in further detail. As a non- migratory, piscivore, this species has previously been used as an indicator of environmental conditions relating to mercury availability (Belger and Forsberg 2006). Regression analysis was used to compare mercury levels across regions while controlling for the weight of the samples caught in each fishing location. Mercury levels on the Corrientes River were lower than on the other two rivers; however, the rate of mercury increase according to body weight was significantly higher on the Corrientes River than in the other two regions. This indicates that the fish on the Corrientes River are bioaccumulating mercury at a faster rate than in other regions. A spill of crude oil, impacting 11,800 m2, had occurred in the

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area where most of our fish samples from the Corrientes River were taken just four and a half months prior to our sampling. The findings point to an increased intake of mercury among the fish that were exposed to crude oil. Since the Corrientes is a region without substantial deforestation, this finding suggests that spills can have a relatively large impact on mercury levels. The fish in the Napo River and the Pastaza River have higher “background” mercury levels resulting from the high rates of deforestation in the upper reaches of each of these watersheds, but spills appear to be contributing to localized bioaccumulation of mercury.

One of the main substantive contributions of this chapter is that it provides information on mercury levels in fish for a region of the Amazon where values had not yet been determined. The significance of this is two-fold: first, this information can be used to help local people who rely on fish reduce their exposure to mercury and, second, this data helps build a complete picture of mercury in Amazonian fisheries, aiding in making comparisons between regions and contributing the first data for an area contaminated by petroleum. Another important substantive contribution is the discovery that an area in which there had recently been an oil spill is an area of heightened bioaccumulation of mercury. This is of singular importance, as this has not been demonstrated in the scientific literature. Whereas Hoplias malabaricus had previously been used as an indicator of natural environmental conditions favouring mercury uptake (Belger and Forsberg 2006), it had not been used as an indicator for environmental contamination. The main methodological contribution of this study is that it demonstrates that this species is sensitive enough to be used in this capacity. This research suffers from two methodological limitations. First, the sample size (35) for the comparison of mercury levels in Hoplias malabaricus is at the lower limit of what is generally accepted for linear regression modelling. Second, only one area that had recently experienced a spill could be studied. While spills happen all too often, they do not occur frequently enough to be captured in replicate in the time frame we had for this study.

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Chapter 4 assesses the levels of organic mercury in local people. Hair samples were collected and interviews were conducted with 192 residents living along the three rivers. Levels of HHg were highest on the Pastaza River (mean: 9.6 μg/g), followed by the Corrientes River (mean: 5.6 μg/g) and, finally, the Napo River (mean: 3.1 μg/g). Mercury levels were found to be contingent on mercury intake, determined primarily by the number of fish meals consumed per week. In one community that had been visited on a previous sampling campaign and that had undergone important changes in livelihood opportunities in the interim, mercury levels and fish consumption were both found to have decreased significantly. Qualitative data from questionnaires indicated that people who live closer to oil operations are more likely to find the quality of fisheries dubious than those who live far away. Concerns range from declining stocks to compromised quality of fish flesh.

The substantive contribution of this research is once again two-fold: first, information particular to individuals and diets can help local people reduce their exposure to mercury; and, second, these data fill a geographic gap in our knowledge of mercury levels in indigenous, riparian communities of Amazonia. Also noteworthy is the contribution that this research makes to the study of the changing health and nutritional status of people with increased livelihood options. Research in Canada has looked at many sides of the diet transition among the Inuit and Cree as they move from country food to market food. Both the declining health status associated with diabetes, heart disease and mental health, and the improved health associated with reduced mercury levels have been documented for these populations. Little academic research has addressed these issues among Amazonian indigenous peoples. This is the first study to look at mercury levels before and after a major diet shift resulting from livelihood changes in the Amazon. Finally, this study contributes to a small body of literature reporting on local people’s deteriorating confidence in the quality of their fisheries as a result of increased contamination. Methodologically, this research combines qualitative

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and quantitative data to build a more complete picture of the changes taking place in the environment and local diet. An important limitation of this chapter was our difficulty in obtaining precise information on fish species consumed. A seven day recall of fish consumption was planned, but the execution of this exercise proved impossible in many cases. This information would have given us more precise figures than the data on most commonly eaten fish species that we were able to obtain for most participants. Having measured participant’s body weight in addition to a seven day recall would have allowed us to calculate the daily mercury intake per body weight, a measure that is often used in such studies.

Inorganic mercury levels in local people and the contribution of oil activities to these levels were addressed in Chapter 5. Samples of urine were collected from a subsample, including 77 people, of the total study population. Levels of urinary mercury (U-Hg) were highest on the Pastaza River (mean: 3.2 μg/g creatinine), followed by the Corrientes River (mean: 3.0 μg/g creatinine) and, finally, the Napo River (mean: 1.9 μg/g creatinine); however, the community with the highest mean concentration of U-Hg, Copal (mean: 4.83 μg/g creatinine), resides on the Corrientes River. Regression analyses, stratified by sex because of important differences in the roles and responsibilities between men and women in indigenous Amazonian households, showed that the only covariate significantly associated with U-Hg concentrations in women is the source of the water they use for washing, whereas the most highly significant covariate in men is whether they had worked for the petroleum companies to clean up the spill that had occurred near two of the communities on the Corrientes River four and a half months prior to sampling. Women who use water from a surface source have two and a half times the amount of mercury (mean: 3.7 μg/g creatinine) in their urine as women who use water from a well, a spring or the rain (mean: 1.4 μg/g creatinine). Men who were involved in the operation to physically remove the crude oil on the surface of lagoons had twice as much mercury in their urine (mean: 3.1 μg/g creatinine) as did those who held other posts (mean: 1.6 μg/g creatinine).

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The role of fish as an important conduit of organic mercury from Amazonian aquatic ecosystems to humans has been amply demonstrated in the scientific literature. Fewer studies have demonstrated the importance of drinking water and water for household use in determining inorganic mercury levels. The substantive contribution of this study is that is shows that women living near petroleum installations have higher U-Hg levels if they use contaminated surface water as opposed to ground or rain water. This study also contributes to the scientific literature on occupational exposure to mercury, revealing that work cleaning up crude oil spills corresponds to elevated exposure. At least one other study has demonstrated that cleaning up oil spills leads to higher mercury concentrations in the urine of workers (Lee et al. 2009b). We were obliged to take only a subsample of the total study population for our research on inorganic mercury for three reasons. First, people were more reluctant to provide a urine sample than they were to provide a hair sample. Women were especially reticent to provide urine. Second, urine samples must be frozen. We were conducting research in remote rainforest areas without electricity so we brought our own mini-bar refrigerator/freezer with our own generator and gas. A larger freezer would not have fit on the boat, nor would the additional gas needed to operate it. The distances were too great for us to have made two trips to the villages. We were, therefore, limited by the physical space in our freezer. Third, urine samples are standardized to creatinine levels. The analysis of creatinine was carried out at the Institut national de santé publique du Québec (INSPQ) at considerable cost. A further limitation of this study relates to the small number of men who had been involved in the clean up of the oil spill.

Chapter 6 assesses 1-hydroxypyrene (1-OHP) levels in local people and the contribution of oil activities to these levels. Urine samples from 75 people were analyzed for 1-OHP. Levels of 1-OHP are higher in this rural population than those reported for most urban populations and populations living near industrial activities elsewhere in the world. The upper range (1.62 μmol/mol creatinine) in the study population exceeds the no-observed-effect-level. Unlike for mercury, no

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significant differences in 1-OHP levels were noted between the three river basins or the eight communities. Regression analyses stratified by sex revealed that, for women, the source of washing water is a significant determinant of 1-OHP levels and, for men, the type of fish most frequently eaten is highly significant. Women who use water from the river or a stream have twice as much 1-OHP in their urine (mean: 0.41 μmol/mol creatinine) as women who obtain their water from either a well, a spring or rain water (mean: 0.22 μmol/mol creatinine). Men who reported eating a bottom-dwelling fish species as their most commonly consumed fish (mean: 0.50 μmol/mol creatinine) had twice as much 1-OHP in their urine as men who reported a pelagic fish (mean: 0.25 μmol/mol creatinine). PAHs are known to settle to the bottom of water bodies where sediments and bottom-dwelling fish become contaminated (Phillips 1999; Boehm and Page 2007). There was no significant difference in the percentage of men and women who consume a bottom-dwelling species most frequently. These findings together point to multiple exposure routes where at least part of PAH uptake is from dermal exposure. Men are responsible for fishing and are exposed to sediments and the fish themselves. Women who use surface water for cleaning spend long periods of time in shallow water washing dishes and clothes. The only health outcome of exposure to petroleum was reported on in an exploratory study in this chapter. The number of miscarriages was found to be significantly, positively associated with 1-OHP levels. An important finding of this research for the health of local people is that women with higher contamination levels are experiencing more miscarriages.

This chapter makes four important substantive contributions to the scientific literature. First, this is the only study reporting on 1-OHP levels in Amazonian populations exposed to crude oil and wastes from the extraction process. Second, these findings provide evidence that women who rely on contaminated surface water for their household work are exposed to pyrene to a greater degree than women who have access to ground or rain water. Few studies on environmental exposure to PAHs have examined exposure via water (Jongeneelen 1994). Third,

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this study indicates that people living near an industrial source of PAHs are exposed to pyrene through fishing and consuming these fish. Fourth, and of particular importance to the epidemiological scientific literature, is the finding that women with greater concentrations of 1-OHP may be experiencing more miscarriages. PAHs are known to have negative outcomes on pregnancies (Sram et al. 2005; Detmar et al. 2006), but this is the first study we know of that relates 1-OHP levels in urine with miscarriages. The limitation of this study is once again a small sample size. Since this was the first time 1-OHP levels were determined for this population, this study was conducted as a pilot project. It is for this reason and the difficulties in collecting urine samples outlined above that this research draws upon a subsample of the total study population. Another limitation of this research was the fact that several women were not able to recall how many miscarriages they had experienced, reducing further the sample size used in the linear regression on miscarriages.

Our strategy to effectively communicate the results of our research to diverse audiences is described in Chapter 7. The emission and biomagnification dynamics of mercury and other contaminants were demonstrated to five of the communities using theater; the parts of oil well, tree, fish, and humans being acted out with costumes by community members. Our experience of using theatre to engage the participants in the process of disseminating our research findings was fruitful. Participants remained attentive throughout the presentation, contributed as volunteer actors, responded to questions, and asked question. Through participants’ correct responses to questions, pertinent queries and the fact that they were able to replicate the information in the form of a game after the play, participants displayed that they comprehended the information we intended to impart. We were continually learning throughout the dissemination process as a result of the question period and fruitful discussions with participants. Finally, the effort put into returning the results of the study was much appreciated by the participants and has translated into increased trust and respect. In light of numerous failures in mercury research communication and the accomplishments

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achieved by this experience, theatre should be considered as a more concrete and dynamic way of imparting the nuanced nature of findings and receiving feedback on research.

Theatre is increasingly used in health research and research teams working on mercury are seeking out innovative and participatory methods of engaging participants and imparting research findings to diverse audiences. This study makes a methodological contribution to the academic literature by demonstrating that theatre can be used to communicate findings from research on mercury. The primary shortcoming of this account is that there is no evaluation component. Because of the limited funding we received and the requirements of doctoral studies it was not possible to return to the field several months after the theatre piece was presented in order to evaluate the efficacy of the activity. How this might have been done is presented in the Discussion and Conclusions of Chapter 7. A second limitation of this research was the low rate of participation by women.

The study design of this doctoral work has made an important methodological contribution to the ecosystem approaches to health field. The theory behind using participatory research, addressing gender and implicating multiple disciplines is well articulated in the literature, but concrete examples of its application are only just now accruing in the mainstream scientific literature. This research integrated all three pillars of the ecosystem approaches to health paradigm. The use of theatre in engaging community members was innovative. The nature of data collection and the use of stratified regression analysis allowed us to speak to gender in a profound way. The integration of a variety of mixed methods – qualitative, quantitative, theatre, and video – and disciplines – geography, ecotoxicology, population health, performance arts and videography – gave this research greater scope than would have been attained through a disciplinary approach.

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8.2 Key Findings The findings of this doctoral research, taken together, point to multiple exposure routes of environmental contaminants in these remote, indigenous populations. It has already been amply demonstrated in other regions of the Amazon basin that deforestation increases mercury levels in aquatic wildlife and people reliant on fish for protein. Since deforestation is a reality in most areas of the Andean Amazon this is undoubtedly an important source of mercury in the study region. However, this research points to another source of mercury in the Andean Amazon – petroleum extraction. Of particular importance in this respect are: (1) the results showing that Hoplias malabaricus from a recently contaminated micro watershed bioaccumulate mercury at a higher rate than Hoplias malabaricus from other regions; and, (2) the discovery that men who were involved in cleaning up an oil spill have higher levels of inorganic mercury than those who were not. Whereas our research does indicate that fish consumption is an important determinant of organic mercury in participants, the same is not the case for inorganic mercury. The source of water for household use and direct contact with crude oil seem to be the most important variables contributing to inorganic mercury levels in the study population.

Our research indicates that these populations are exposed not only to relatively high levels of mercury but also to PAHs. In the absence of urban exposure or other industrial inputs, the primary source of PAHs to the region is petroleum extraction. The evidence points to multiple exposure routes for local populations including drinking water, contaminated fish and dermal uptake from sediments laden with PAHs. The findings of particular importance in drawing this conclusion are: (1) the fact that women who use surface water as opposed to ground or rain water have higher levels of 1-OHP in their urine; and, (2) that men who eat more bottom-dwelling fish have a greater concentration of 1-OHP in their urine. Qualitative data corroborates these findings. Local people’s traditional knowledge and current observations have led many of them to the conclusion that the activities of petroleum companies in the area are contributing to a

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deterioration of fisheries. This is a particularly important finding in light of the fact that women with higher levels of 1-OHP reported more miscarriages. Our research shows that at least one of the negative health outcomes associated with exposure – miscarriages – is related to the presence of PAHs in the body. These results combined can be used to encourage petroleum companies to provide wells to all communities located on contaminated rivers in order to reduce the number of miscarriages experienced by women.

The policy implications of this research are elaborated in depth in each of the separate chapters. Here, some of the more salient recommendations are summarized. In order to minimize mercury transfer to aquatic ecosystems, forest conservation strategies would be best concentrated within the Pastaza Megafan. Several sizeable protected areas in the Pastaza and Corrientes River Basins and on the southern side of the Napo River Basin are recommended. Riparian protected areas are also encouraged. Laws exist that require companies to re-inject production waters and cease using open flares. Independent verification that companies are complying with the law is necessary. More care must be taken to avoid spills. Spills and abandoned waste sites need to be thoroughly cleaned up; otherwise they are a continuing source of contamination to water bodies. Petroleum companies must require workers who are in direct contact with crude oil to wear the appropriate protective gear. We recommend that the petroleum companies provide wells to all communities that are likely impacted by oil contamination, including communities located at a distance from oil operations. In the meantime rain water and springs should be prioritized as the main sources of water.

While no one would argue against poverty reduction in one of the most isolated and impoverished areas of the world, strategies to increase incomes and access to health care, education and other commodities should be implemented with care. Economic development in the Andean Amazon, based as it is on the extraction of oil and frontier agricultural activities, is a growing health concern. Soil erosion

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from cleared plots leads to mercury contamination of one of the most nutritious and most sustainable local food sources – fish. Oil pollution contributes to mercury levels and releases hydrocarbons into these remote watersheds. The direct negative health outcomes of exposure to these contaminants include neurological damage, cancer and miscarriages. The negative health outcomes associated with the nature of land use in the area are broader and span the social and emotional dimensions of life. Synergies between contaminants and the combination of multiple negative impacts could lead to unknown consequences. Exposure over the entire course of a lifetime – beginning in the womb and continuing past the working years – could also lead to impacts different from what has been documented in the literature. The precautionary principle entreats us to implement development strategies with caution. The health of the people indigenous to these lands should take precedence over economic interests.

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Appendix 1: Questionnaire

Fecha ______Comunidad ______

La deforestación puede provocar la erosión de los suelos de la orilla hasta el río. Hay mercurio en los suelos. Cuando los seres humanos comen pescado puede consumir mercurio también. El mercurio puede dañar la salud. Estamos haciendo un estudio para ver la cantidad de mercurio en el pescado del Río y los habitantes de su comunidad. Queremos saber las fuentes de mercurio y cuales peces tienen más mercurio. Estamos interesados en la dieta de la gente y su uso de la tierra. Quisiéramos saber si usted estaría interesado(a) en participar en el estudio. Su participación sería para responder la encuesta que sigue y para facilitarnos una muestra de su cabello y en algunos casos la orina. Su participación no representa ningún peligro para su salud ni para su integridad y la información será reservada. No hay ninguna recompensa por su participación. ¿Tiene Ud. preguntas?

Yo______identificada con D.N.I. N°______manifiesto que:

Estoy informada del estudio de investigación que realizará la investigadora Jena Webb de la Universidad McGill. Ante lo expuesto, DOY MI CONSENTIMIENTO INFORMADO para participar en dicho estudio, brindando información confiable la misma que será tratada con total confidencialidad para fines del estudio.

En conformidad con lo expresado, dejo constancia mi firma y/o huella digital.

____ de ______de 2006 ______FIRMA JENNIFER WEBB

1 Informaciones Personales 1.1 Nombre ______1.2 Sexo (F) (M) 1.3 Edad ______1.4 Grupo social ______1.5 Ocupación ______1.6 Escolaridad: Ninguna ( ) Primaria incompleta ( ) Primaria completa ( ) Secundaria ( ) Superior ( ) 1.7 ¿Sabe Ud. Leer/escribir? ( ) No ( ) Sí 1.8 ¿Cuanto tiempo vive Ud. aquí?______1.9 ¿Dónde vivía Ud. antes? ______

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1.10 ¿Cuántos niños tiene Ud.? ______1.10.1 ¿Cuántos años tiene el mayor? ______¿Y el menor? ______1.10.2 Por madres: ¿Hasta qué edad amamanta Ud. sus niños? ______(años) 1.10.3 ¿Tuvo Ud./tu mujer abortos? ( ) No ( ) Sí → ¿A cuántas meses? ______1.10.4 ¿Algún hijo suyo se murió? ( ) No ( ) Sí → ¿De qué? ______

2 Salud 2.1 ¿Ud. fuma? ( ) No ( ) Sí → ¿Cuántas cigarrillos por día? ______(cigarrillos) 2.2 ¿Ud. toma? ( ) No ( ) Sí → ¿Qué toma Ud.? ______2.2.2 ¿Cuántas cervezas/tragos por día? ______(cervezas) ______(tragos)

2.3 ¿Tiene Ud. alguna(s) enfermedad(es)? ( ) No (→ 2.4) ( ) Sí → ¿Cuál(es)?

2.4 ¿Tiene Ud. problemas respiratorios? ( ) No (→ 2.5) ( ) Sí → ¿Cuándo?

2.5 ¿Tiene Ud. problemas digestivos? ( ) No (→ 2.6) ( ) Sí → ¿Cuándo?

2.6 ¿Tiene Ud. problemas cardiovasculares? ( ) No (→ 2.8) ( ) Sí → ¿Qué tipo?

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2.7 ¿Tiene Ud. erupciones cutáneas? ( ) No (→ 2.10) ( ) Sí → ¿Dónde/cuándo?

2.8 ¿Tiene Ud. mareo? ( ) No (→ 2.11) ( ) Sí → ¿Cuándo? ______

2.9 ¿Tiene Ud. problemas con su visión? ( ) No (→ 2.12) ( ) Sí → ¿Cuándo/qué tipo?

2.10 ¿Alguien en su familia tuvo/tiene el cáncer? ( ) No (→ 2.14) ( ) Sí → ¿Quién/cuándo/qué tipo?

3 Trabajo 3.1 Oro ¿Practica Ud. o alguien en su familia la extracción del oro? ( ) No (→ 3.2) ( ) Sí → 3.1.1 ¿Quién? ______3.1.2 ¿De dónde saca el oro? ______3.1.3 ¿Cómo lo saca? ______

3.1.4 ¿Usa ( ) mercurio (→ 3.1.5) ( ) cianuro otro ______? 3.1.5 ¿Quema el mercurio? ( ) No (→ 3.1.6) ( ) Sí → ¿Cómo?______

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3.1.6 ¿Usa protección? ( ) mascarilla ( ) guantes otro ______3.1.7 ¿Cómo bota los desechos del proceso? ______

3.2 Trabajo en las Compañías Petroleras 3.2.1 ¿Ya ha trabajado Ud. o alguien en su familia por las compañías petroleras? ( ) No (→ 4) ( ) Sí → ¿Quién? ______3.2.2 ¿Hace cuánto tiempo? ______3.2.3 ¿Por cuánto tiempo? ______3.2.4 ¿Qué cargo hacía? ______3.2.5 ¿Trabajaba con el petróleo directamente? ( ) No (→ 3.2.6) ( ) Sí → ¿Cómo? ______3.2.6 ¿Trabajaba con productos químicos? ( ) No (→ 4) ( ) Sí → ¿Cuáles? ______

4 La Pesca 4.1 ¿Dónde va Ud. para pescar? ( ) El Río ( ) La Cocha ( ) Una quebrada ( ) Otro ______

4.2 ¿Va Ud. cerca de los pozos para pescar? ( ) No (→ 4.6) ( ) Sí → 4.2.1 ¿Dónde? ______

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4.2.2 ¿Con qué frecuencia? ______4.2.3 ¿Qué tipo de peces pesca Ud. allá (si diferente que lo normal)? ______4.3 ¿Va Ud. cerca de un oleoducto para pescar? ( ) No (→ 4.7) ( ) Sí → 4.3.1 ¿Dónde? ______4.3.2 ¿Con qué frecuencia? ______4.3.3 ¿El tipo de peces que pesca Ud. allá es diferente? ______

4.4 ¿Compra Ud. pescado? ( ) No (→ F.12) ( ) Sí → 4.4.1 ¿Dónde/de quién lo compra? ______4.4.2 ¿Qué tipo de pescado? ______

4.5 ¿Ha notado algunos cambios en los peces en los últimos años? ( ) No (→ 5) ( ) Sí → 4.5.1 ¿Cuáles?______

4.6 ¿En relación a hace 10 años, la pesca ahora es: ( ) Mejor ( ) Peor ( ) Igual 4.6.1 En su opinión, ¿por qué? ______

5 La Dieta 5.1 Pescado 5.1.1 ¿Cuantas veces come Ud. pescado a la semana? ______veces

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5.1.2 ¿Qué pescados come Ud. con más frecuencia? (1) ______(2) ______(3) ______Otros:

5.1.3 ¿Qué cantidad de pescado come Ud. normalmente? ______(¿De qué tamaño son los pescados normalmente?) 5.1.4 ¿En relación a hace 10 años, Ud.: ( ) ¿Come más pescado? (→ 5.1.9) ( ) ¿Come menos pescado? (→ 5.1.9) ( ) ¿Come pescado igual? (→ 5.2) 5.1.5 ¿Por qué? ______

5.2 Animales salvajes/Aves/ Animales acuáticos (lagarto, tortugas, etc.) 5.2.1 ¿Come Ud. carne de monte? ( ) No (→ B) ( ) Sí → 5.2.2 ¿Cuáles? ______

5.2.3 ¿Cuántas veces a la semana come Ud. carne de monte? ______veces 5.2.4 ¿En relación a hace 10 años, Ud.: ( ) ¿Come más carne de monte? (→ 5.2.A8) ( ) ¿Come menos carne de monte? (→ 5.2.A8)

( ) ¿Come carne de monte igual? (→ B) 5.2.8 ¿Por qué? ______

5.3 Animales domésticos

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5.3.1 ¿Con qué frecuencia come Ud.: pollo ______carne de res ______cerdo ______pavo ______pato ______otro ______?

5.4 Frutas 5.4.1 ¿Con qué frecuencia come Ud.: guaba______papaya ______guanábana ______piña ______limón ______naranja ______mango ______toronja ______banano ______nuez de brasil ______otro______

5.5 Agua 5.5.1 ¿De dónde saca Ud. el agua que toma? ______5.5.2 ¿De dónde saca Ud. el agua que usa para cocinar? ______5.5.3 ¿De dónde saca Ud. el agua que usa para laver/banarse? ______5.5.4 ¿Toma Ud. agua hervida? ( ) No ( ) Sí

5.6 Comida comercial

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5.6.1 ¿Compra Ud. algunas comidas (atún, sardinas)? ( ) No ( ) Sí → ¿Cuáles y con qué frecuencia? ______

¡Muchas Gracias!

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Appendix 2: Mercury Levels in Resident, Predatory, Amazonian Fish Species and Comparison with Results of Previous Studies

Table A1 summarizes mercury levels in resident, predatory fish reported in the scientific literature. Studies in which the results are given in dry weight are not considered here (Boudou et al. 2005; Durrieu et al. 2005; Régine et al. 2006). Few reference levels from control sites have been reported.

For Cichla spp. (tucunaré) our samples had lower mercury levels than all those summarized here except those caught at Cachoeira do Piria, Brazil, a gold mining region, although no indication of the size of the fish is given in the article (Palheta and Taylor 1995). The weight of our 5 specimens (μ = 620g) falls at the lower end of most of the articles that reported this measure with the exception of Sai Cinza (da Silva Brabo et al. 2000), Santarém (de Souza Lima et al. 2000), and Itaituba (Santos et al. 2000) on the Tapajós River, Brazil. The levels found in the Corrientes region (Atilliana and Piuri lagoons) were slightly higher than a control site on the heavily deforested Tapajós River (Castilhos et al. 1998), a clear water river. The levels in our samples were notably lower than at control sites in Suriname (Mol et al. 2001) and Amapa, Brazil (Guimaraes et al. 1999); however, these are clear and black waters (Silva-Forsberg et al. 1999).

For Hoplias malabaricus (fasaco/guanchiche), likewise, our samples have lower concentrations of mercury than reported in the literature. Specimens of Hoplias malabaricus that we caught at sites on the Pastaza River were smaller than those in the majority of the articles listed here, but those from sites on the Corrientes and the Napo are similar in size. Our findings show levels that are slightly higher than those reported from “control” sites on the Tapajós River, but again, the Tapajós River might be better considered as being contaminated along its length owing to the rapid rate of land use change occurring along the banks.

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Our specimen of Hydrolycus scomberoides (huapeta), caught in Capahuari Lagoon on the Pastaza River, was considerably smaller than those reported in the literature and only slightly less contaminated in mercury, except in Santarém (de Souza Lima et al. 2000). The values found in Pygocentrus nattereri (pana roja) in sites along the Napo River were lower than those reported in three of the studies examined here. Fish caught on the Beni River were extremely large (Maurice- Bourgoin et al. 2000a) but the range of standard lengths of our specimens (9.5 to 32 cm) overlapped those reported by Sampaio da Silva et al. (2005). The mean mercury concentration for this species on the Bento Gomes River, a gold mining region in the Panatanal, Brazil, on the other hand, was considerably lower than what we found (Lacerda et al. 1991). The authors offer a possible reason for such low levels in a region draining tailings from gold mining: water flow is extremely high, effectively diluting the amount of mercury in the ecosystem.

Mercury concentrations in our specimens of Rhaphiodon vulpinus (chambira/pez perro), on the other hand, are comparable with those described in the literature: the mean mercury concentration for this species caught at sites on the Napo region (0.629 μg/g) was in one case higher (0.37 μg/g, Lebel et al. 1997b) and in another the same as (0.624 μg/g, Castilhos et al. 1998) that given for the Tapajós River. Rhaphiodon vulpinus from the Napo region has less mercury than on the Madeira River (Boischio and Henshel 2000b), despite being of similar size. The results from the Pastaza region place this fish higher in mercury content than reported by Lebel et al. (1997b), but lower than the rest, although these specimens were also smaller in size.

The carnivore Crenicichla sp. (anashua/vieja) displays lower mercury levels in our study regions than in the gold mining Tapajós and Madeira Rivers, but our samples are substantially smaller (77 vs. 300g). The carnivore Pimelodus blochii (cunchi/barbudo) was less contaminated than all the studies reported except for the gold mining regions Cachoeira do Piria, Brazil (Palheta and Taylor 1995) and the Beni River, Bolivia (Maurice-Bourgoin et al. 1999) where the values are

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similar; but, once again, in the one article that reports the weight of the fish (Maurice-Bourgoin et al. 2000a) our samples are considerably smaller. The white piranha, Serrasalmus rhombeus, displays a similar pattern on the Napo River: the mean mercury concentration is less than in most other studies but the fish caught were half as large; this is even the case for the reference level in Suriname (Mol et al. 2001); however, as mentioned above, this reference level is probably irrelevant for the upper Amazon due to important differences in water chemistry. The exception comes once again from Bento Gomes River, Brazil, where the high water flow rate dilutes mercury from gold mining (Lacerda et al. 1991). Black Piranha, Serrasalmus spilopleura, on the other hand, is larger on all three rivers studied here than in the literature and has considerably more mercury.

The omnivore Brycon melanopterus (sabalo) in both the Napo and Pastaza regions exhibited greater mercury concentrations than on the Tapajós (Castilhos et al. 1998) and the Beni (Maurice-Bourgoin et al. 2000a) Rivers, but similar or less than reported on the Madeira River, including putative control site (Malm et al. 1989; Pfeiffer et al. 1991; Boischio and Henshel 2000b). There is no clear trend for the omnivore Leporinus friderici (lisa). Our specimens from the Corrientes are smaller in size but higher in mercury than those reported from Santarém (de Souza Lima et al. 2000) and Itaituba (Santos et al. 2000); otherwise, they are lower in mercury, except for on the Bento Gomes River, where no weights are given and mercury concentrations were below the detection limit. All of our sample means are lower than the reference level given for black and clear waters in Suriname (Mol et al. 2001). Finally, our specimens of Triportheus angulatus (sardina) from the Corrientes and especially the Pastaza region are smaller in size than but comparable to or higher in mercury than the studies summarized here except for the study carried out in French Guiana where they found higher concentrations (Richard et al. 2000).

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Table A1: Reported mercury levels (μg/g) in resident, predatory, Amazonian fish species.

Species Article Region n Weight Hg concentration (mean or (mean or range) range) (g) (μg/g) Piscivores Cichla spp. Belger and Forsberg (2006) Negro River, Brazil 50 809 0.337 (0.031-1.469) Tucunaré Dorea et al. (2006) Negro River, Brazil 112 192–2100 0.039-2.44 (peacock bass) Kehrig et al. (2008) Negro River, Brazil 5 350-570 0.38 da Silva Brabo et al. (2000) Sai Cinza, Tapajós River, Brazil 17 340-550 0.267 de Souza Lima et al. (2000) Santarém, Tapajós River, Brazil 10 503 0.306 Santos et al. (2000) Itaituba, Tapajós River, Brazil 10 530 0.375 (0.214-0.61) Sampaio de Silva et al. Tapajós River, Brazil 11 28-62 cm 0.45-0.538 (2005) Uryu et al. (2001) Santarém, Tapajós River, Brazil 34 - 0.175 Bidone et al. (1997b) Tapajós River, Brazil 33 - 0.42 Lebel et al. (1997b) Tapajós River, Brazil 6 0.4 (0.21-0.75) Castilhos et al. (1998) Tapajós River, Brazil (Au-mine 33 - 0.42 site) Castilhos et al. (1998) Tapajós River, Brazil (control 28 - 0.116 site) Kehrig et al. (2008) Tapajós River, Brazil 42 250-4800 0.55 Pfeiffer et al. (1991) Jaci Paraná (Madeira), Brazil - - 0.47 Kehrig et al. (2008) Madiera River, Brazil 8 216-937 0.47 Bastos et al. (2006) Madiera River, Brazil 167 - 0.414 Boischio and Henshel Madeira River, Brazil 22 720 0.66 (0.12-2.21) (2000b) Malm et al. (1989) Jaci Parana River - - 0.47 Bidone et al. (1997a) Tartarugalzinho River, Brazil 6 - 0.441 Palheta and Taylor (1995) Cachoeira do Piria, Brazil 3 - 0.11 Hacon et al. (1997a) Alta Floresta, Brazil 11 - 0.28 Guimaraes et al. (1999) Amapa State, Brazil (Au-mine ~24 250-2500 0.261 site) Guimaraes et al. (1999) Amapa State, Brazil (control site) ~16 125-900 ~0-1.0 Eve et al. (1996) Iranduba and Barreirinha, Brazil - - 0.51 Kehrig and Malm (1999) Balbina Resevoir, Brazil 17 - 0.06-0.73 Kehrig et al. (2008) Tucuruí reservoir, Brazil 19 108-985 0.49

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Porvari (1995) Tucuruí reservoir, Brazil 53 200-4500 1.1 Reuther (1994) Rio Jamari (reservoir), Brazil 2 - 0.53 Mol et al. (2001) Suriname (Au-mine sites) 52 794 0.72 (0.16-2.52) Mol et al. (2001) Suriname (control site) 3 811 0.39 (0.25-0.57) Richard et al. (2000) French Guiana 1 1300 0.22 Hoplias malabaricus Belger and Forsberg (2006) Negro River, Brazil 46 4-1594 0.35 (0.055-1.008) Fasaco / Guanchiche Dorea et al. (2006) Negro River, Brazil 18 240-596 0.12-1.54 da Silva Brabo et al. (2000) Sai Cinza, Tapajós River, Brazil 7 400-775 0.322 Uryu et al. (2001) Santarém, Tapajós River, Brazil 6 - 0.133 Uryu et al. (2001) Tapajós River, Brazil 6 - 0.550-1.105 Bidone et al. (1997b) Tapajós River, Brazil 4 - 0.62 Lebel et al. (1997b) Tapajós River, Brazil 1 - 0.49 . Castilhos et al. (1998) Tapajós River, Brazil (control 10 - 0.102 site) Boischio and Henshel Madeira River, Brazil 14 420 0.38 (0.08-1.06) (2000b) Pfeiffer et al. (1991) Madeira River, Brazil - - 0.36-0.6 Reuther (1994) Rio Mutum Parana, Brazil 2 - 0.83 Bidone et al. (1997a) Tartarugalzinho River, Brazil 2 - 0.335 Palheta and Taylor (1995) Cachoeira do Piria, Brazil 13 - 0.61 Lima et al. (2005) Cachoeira do Piria, Brazil 35 270 0.882 Hacon et al. (1997b) Alta Floresta, Brazil 8 - 0.36 Guimaraes et al. (1999) Amapa State, Brazil (Au-mine 7 250-2800 0.549 site) Guimaraes et al. (1999) Amapa State, Brazil (control site) 9 250-700 ~0.1-1 Mol et al. (2001) Suriname (Au-mine sites) 25 280 0.52 (0.24-0.96) Richard et al. (2000) French Guiana 3 510-1068 0.5 (0.43-0.58) Hydrolycus sp. Dorea et al. (2006) Negro River, Brazil 83 19–783 0.114-5.437 Huapeta de Souza Lima et al. (2000) Santarém, Tapajós River, Brazil 10 442 0.124 Lebel et al. (1997b) Tapajós River, Brazil 1 - 0.52 Castilhos et al. (1998) Tapajós River, Brazil 5 - 0.69 Maurice-Bourgoin et al. Beni River, Bolivia 5 2500-3900 0.989 (0.5341.485) (2000a) Maurice-Bourgoin et al. Beni River, Bolivia 3 - 0.806-1.087 (1999) Pygocentrus nattereri Sampaio de Silva et al. Tapajós River, Brazil 17 11-23 cm 0.367-0.403 (2005) Pana Roja Lebel et al. (1997b) Tapajós River, Brazil 5 - 0.55 (0.41-0.67) Maurice-Bourgoin et al. Beni River, Bolivia 2 1170-1200 1.219 (1.206-1.233)

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(2000a) Lacerda et al. (1991) Bento Gomes River, Pantanal, - - 0.06 Brazil Rhaphiodon vulpinus Boischio and Henshel Madeira River, Brazil 10 500 0.87 (038-1.08) (2000b) Chambira / Pez Lebel et al. (1997b) Tapajós River, Brazil 2 - 0.37 (0.31-0.42) Perro Castilhos et al. (1998) Tapajós River, Brazil 4 - 0.624 Carnivores Crenicichla sp. Lebel et al. (1997b) Tapajós River, Brazil 1 - 0.27 Anashua / Vieja Castilhos et al. (1998) Tapajós River, Brazil 3 - 0.47 Boischio and Henshel Madeira River, Brazil 4 300 0.79 (0.41-1.25) (2000b) Pimelodus blochii Bidone et al. (1997b) Tapajós River, Brazil 5 - 0.28 Cunchi / Barbudo Lebel et al. (1997b) Tapajós River, Brazil 2 - 0.3 (0.26-0.35) Castilhos et al. (1998) Tapajós River, Brazil 5 - 0.28 Bastos et al. (2006) Madiera River, Brazil 41 - 0.248 Palheta and Taylor (1995) Cachoeira do Piria, Brazil 6 - 0.18 Maurice-Bourgoin et al. Beni River, Bolivia 1 260 0.48 (2000a) Maurice-Bourgoin et al. Beni River, Bolivia 1 - 0.125 (1999) Serrasalmus rhombeus Dorea et al. (2006) Negro River, Brazil 71 35–443 0.063-1.085 Pana Blanca Lebel et al. (1997b) Tapajós River, Brazil 11 - 0.53 (0.07-1.12) Kehrig and Malm (1999) Madeira River, Brazil 10 - 0.69 Kehrig et al. (1998) Balbina Resevoir, Brazil 4 Some over 0.6 600 Mol et al. (2001) Suriname (Au-mine sites) 88 761 1.15 (0.31-4.62) Mol et al. (2001) Suriname (control site) 8 633 0.35 (0.18-0.59) Richard et al. (2000) French Guiana 80 80-2600 0.42 (0.05-1.37) Lacerda et al. (1991) Bento Gomes River, Pantanal, - - 0.06 Brazil Serrasalmus Lebel et al. (1997b) Tapajós River, Brazil 11 - 0.4 (0.09-0.59) spilopleura Pana Negra Maurice-Bourgoin et al. Beni River Basin, Bolivia 1 120 0.049 (2000a) Omnivores Brycon sp. Castilhos et al. (1998) Tapajós River, Brazil 3 - 0.052 Sabalo Boischio and Henshel Madeira River, Brazil 6 340 0.17 (0.08-0.26)

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(2000b) Malm et al. (1989) Jamari River, Brazil (control site) - 520 0.08 Pfeiffer et al. (1991) Jamari River, Brazil (control site) - - 0.08 Maurice-Bourgoin et al. Beni River, Bolivia 1 830 0.034 (2000a) Leporinus friderici Dorea et al. (2006) Negro River, Brazil 27 135–515 0.017-0.219 Lisa de Souza Lima et al. (2000) Santarém, Tapajós River, Brazil 10 384 0.068 Santos et al. (2000) Itaituba, Tapajós River, Brazil 13 356 0.065 (0.027-0.126) Lebel et al. (1997b) Tapajós River, Brazil 32 - 0.08 (0.03-0.37) Lima et al. (2005) Cachoeira do Piria, Brazil 38 60 0.124 Mol et al. (2001) Suriname (Au-mine sites) 3 102 0.25 (0.2-0.31) Mol et al. (2001) Suriname (control site) 1 282 0.09 Richard et al. (2000) French Guiana 90 152-3600 0.114 (0.007-0.47) Lacerda et al. (1991) Bento Gomes River, Pantanal, - - <0.04 Brazil Triportheus spp. Dorea et al. (2006) Negro River, Brazil 13 92–308 0.013-0.135 Sardina Lebel et al. (1997b) Tapajós River, Brazil 6 - 0.13 (0.02-0.3) Bastos et al. (2006) Madeira River, Brazil 31 - 0.231 Boischio and Henshel Madeira River, Brazil 18 160 0.15 (ND-0.57) (2000b) Maurice-Bourgoin et al. Beni River Basin 46 81-315 0.099 (0.01-0.28) (2000a) Richard et al. (2000) French Guiana 3 510-1068 0.5 (0.43-0.58) n = Number of fish analyzed

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Appendix 3: Reported Concentrations of Mercury in Urine of Populations from the Amazon and Andean Foothills

Table A2: Reported concentrations of mercury in urine in populations from the Amazon and Andean foothills. Country Source of Exposure Exposed Population U-Hg concentration Reference (μg/l)*† Occupational Brazil Gold mining Miners 25.3 Barbosa et al. (1995) Brazil Gold mining Miners 1-155 Palheta and Taylor (1995) Peru Gold mining Workers in smelters 728 (321-1662) Hurtado et al. (2006) Peru Gold mining Workers in amalgamation 18 (8-37) Hurtado et al. (2006) Brazil Gold mining and Workers 32.7 (0-151) Branches et al. (1993) shops Brazil Gold shops Workers in gold shops 2.9-225 Santa Rosa et al. (2000) Brazil Gold shops Managers, burners, cashiers 57.5 (27-663) Jesus et al. (2001) Brazil Gold mining Miners 6.4 (0-74.3) Jesus et al. (2001) Ecuador Gold washing Child labourers 52.1 (26-159) Harari et al. (1997) Ecuador Gold mining Child labourers 10.9 (1-166) Counter et al. (2005) Environmental Peru Gold mining Living near smelter 113 (45-197) Hurtado et al. (2006) Peru Gold mining Living in mining town 8 (5-10) Hurtado et al. (2006) Peru Gold mining Living outside mining town 4 (2-6) Hurtado et al. (2006) Dietary Brazil Fish Riparian fish-eating 14 Barbosa et al. (1995) population Brazil Fish Riparians 1-2.5 Palheta and Taylor (1995) Brazil Fish Riparian fish-eating 7.5 (0.2-36.1) Passos et al. (2007b) population Notes: * range or mean unless otherwise indicated † note that the U-Hg levels in these studies were not standardized to creatinine levels

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Appendix 4: Reported Concentrations of 1-OHP in the Literature

Table A3: Reported concentrations of 1-OHP in the literature: location of the study, type of exposure, study population, 1-OHP concentration and reference. Country/city Source of Exposed Population 1-OHP concentration Reference Exposure (μmol/mol creatinine)* Urban Netherlands Traffic Adults, non-smokers 0.04-0.29 Van Rooij et al. (1994) Germany Traffic Adults, non-smokers 0.06–0.46 Scherer et al. (2000) Tokyo Traffic Children 0.039–0.076 Kanoh et al. (1993) the Czech Traffic Children 0.01-1.426 Fiala et al. (2001) Republic the Czech Traffic Adults, smokers and 0.01-0.7 Vyskocil et al.(1997) Republic non-smokers Denmark Traffic Children 0.01-0.63 Hansen et al. (2005) Spain Traffic Pregnant women 0.05 (median) Llop et al. (2008) Spain Traffic Children 0.004-0.314 Freire et al. (2009) The United Traffic Nationally 0.024 Li et al. (2008) States representative sample The United Traffic Adults, smokers and 0.02 Suwan-ampai et al. States non-smokers (2009) New Zealand Traffic Boys on high pollution 0.006-0.724 Cavanagh et al. (2007) days Bangkok Traffic Children 0.05-1.48 Ruchirawat et al. (2007) Italy Traffic Adults, smokers and 0.056-0.21 (interquartile Cocco et al. (2007) non-smokers range) Milan Traffic Adults (27% smokers) 0.08±0.08 μmol/mol Pastorelli et al. (1999) Korea Traffic Middle School children 0.01-1.23 Kang et al. (2002) Industrial Poland Nearby coal/coke Non-smokers 0.13-0.38 Ovrebo et al. (1995) industry Poland Nearby coal/coke Children 0.04–1.95 Mielzynska et al.

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industry (2006) Netherlands Living on coal Children 0.03-6.39 van Wijnen et al. tailings (1996) Germany Coal industry Female, non-smokers 0.15 (median) Gündel et al. (1996) Belgium Nearby chemical Female, non-smokers 0.008-0.092 van Larebeke et al. and petrochemical (2006) industry Belgium Combined urban Adults (smokers and 0.074 (median) De Coster et al. (2008) and industrial non-smokers) Belgium Combined urban Adolescents 0.0068-0.32 Schroijen et al. (2008) and industrial Canada Nearby creosote Adults, non-smoking 0.01-0.17 Bouchard et al. (2001) impregnation factory Korea Nearby steel mill Children 0.040 ± 2.647 Lee et al. (2009a) Australia Living on an old Adults, smokers and 0.03-0.1 Turczynowicz et al. gasworks site non-smokers (2007) Indoor air quality Poland Coal heating (no Children 0.21–0.40 Siwinska et al. (1999) environmental tobacco smoke) Mexico Wood burning Adults and children, 1.1-17.8 Torres-Dosal et al. smokers and non- (2008) smokers Burundi Wood burning Adults, smokers and 0.26-15.62 Viau et al. (2000) non-smokers China Cooking without a Women 0.75 Chen et al. (2007) fume extractor Water Netherlands Contaminated Adults, smokers and 0.16-0.81 Jongeneelen (1994) recreation water non-smokers Notes: * range or mean unless otherwise indicated

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