Long-Term Changes to Food Web Structures and Mercury Biomagnification in Three Large, Inland
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Long-term changes to food web structures and mercury biomagnification in three large, inland North American lakes By John Poulopoulos A thesis submitted to the Department of Biology in conformity with the requirements for the Degree of Doctor of Philosophy Queen’s University Kingston, Ontario, Canada January 2013 Copyright © John Poulopoulos, 2013 Abstract Numerous anthropogenic disturbances have occurred in large lakes over recent decades. These may alter concentrations of the biomagnifying contaminant mercury (Hg) in fish, but long-term impacts of disturbances on Hg trophodynamics are poorly understood. Elemental analyses of archived museum ichthyology specimens could be used to study historical, pre-disturbance fish food webs, but there is uncertainty about effects of chemical preservatives on the results of such analyses. In this thesis, long-term preservation effects were studied, and archived fish were used to reconstruct historical food webs and Hg trophodynamic patterns in three large North American lakes, Nipigon, Simcoe and Champlain. After 24 months of formalin/ethanol preservation, fish muscle 15N and 13C had average changes of +0.4 ‰ and -0.9 ‰, respectively. Shifts in mean Hg concentration was +5 % after 12 months. A suite of 26 other elements analyzed over 24 months showed consistent responses to preservation, usually involving an increase in concentration immediately following preservation. In the second phase of the thesis, stable isotope and Hg analyses were performed on archived and modern fish from the study lakes, dating to the 1920s-60s and 2006-7, respectively. Trophic relationships were often relatively stable over time, but stable isotope metrics revealed a decrease in Lake Nipigon 15N range and less pelagic feeding among Lake Simcoe pumpkinseed and yellow perch. In Lake Champlain, the re-introduction of lake trout in recent decades did not have a major effect on overall food web dimensions. Significant Hg biomagnification factors were found in 1920s and 2006-7 Lake Nipigon (which were not statistically distinguishable from each other) and 2006 Lake Champlain. These biomagnification ii factors ranged from 0.09 to 0.17, which is within the range found in other studies globally. Archived fish and government monitoring records indicated that fish Hg concentrations decreased in Lakes Simcoe and Champlain since historical periods, but remained similar or increased in Lake Nipigon. This thesis confirms the utility of archived fish for elemental analyses. It highlights the risks of Hg contamination and food web change that may be faced by remote lakes, and it provides evidence for relatively stable Hg biomagnification rates in large lakes. iii Statement on Co-authorship Chapters 2-4 (manuscripts) were co-authored with my supervisor, Linda M. Campbell, and with T. Kurtis Kyser who directs the Queen’s Facility for Isotope Research. I was primarily responsible for all aspects of the project, including overall study design, field sampling, laboratory sample preparation and analysis, statistical analyses, and writing of manuscripts. Drs. Campbell and Kyser provided guidance and training on these topics through regular meetings, review of my analyses, and comments on manuscripts. iv Acknowledgements I would first like to thank my parents, friends and family, whose support during this project was too great to describe. I was fortunate to have numerous people to help me at Queen’s, including my supervisor, Linda Campbell; my summer assistants, Deirdre Allen and Patrick Mislan; Kurt Kyser and Kerry Klassen in the isotope lab; my supervisory committee members, Peter Hodson, Shelley Arnott, and Tim Johnson; Carolyn Glass, whose project opened the door for my own; Alemayehu Asfaw in the Dept. of Chemistry; and the rest of my lab mates. I also received generous assistance and/or data from colleagues at other institutions, including Ellen Marsden (Univ. of Vermont); Rick Salmon, Albertina van Ogtrop, and Jake La Rose (Ont. Ministry of Natural Resources); Erling Holm (Royal Ontario Museum); Douglas Nelson (Univ. of Michigan Museum of Zoology); and Richard Langdon (NY State Museum); Emily Awad (Ont. Ministry of Environment); and Neil Kamman (Vermont Dept. of Environmental Conservation). I received funding from the Queen’s University Graduate Dean’s Travel Grant for Doctoral Field Research, Queen’s University Graduate Award, and International Association for Great Lakes Research Scholarship. My research was also funded by an NSERC Discovery research grant, Ontario Early Researcher Award and Queen’s University Chancellor Research Award to Linda Campbell. The Queen’s Facility for Isotope Research is supported by grants from the Canada Foundation for Innovation, the Ontario Innovation Fund and the Natural Sciences and Engineering Research Council of Canada. v Table of Contents Abstract…………………………………………………………………………..… ii Statement on co-authorship…………………………………………………………iv Acknowledgements………………………………………………………………… v Table of contents…………………………………………………………………… vi List of Tables…………………………………………………………………….… viii List of Figures……………………………………………………………………… ix List of Abbreviations………………………………………………………….…… xi Chapter 1: General introduction……………………..…………………………...…1 1.1: Changes to lake food webs………………………………………….… 1 1.2: Mercury in the environment………………………………………...… 2 1.3: Retrospective chemical tracer analyses……………………………….. 4 1.4: Project outline…………………………………………………….…… 6 1.5: Thesis objectives…………………………………………………….… 8 Chapter 2: Preservation effects on stable isotopes, total and methyl Hg, and 26 other elements in archived fish tissue……….……………………………………... 9 2.1: Abstract…………………………………………………………...…… 9 2.2: Introduction……………………………………………………….…… 10 2.3: Methods……………………………………………………………..… 13 2.4: Results……………………………………………………………….… 20 2.5: Discussion……………………………………………………………... 21 vi Chapter 3: Stable isotope analyses reveal long-term food web changes in large inland lakes of North America……………………………………………………... 48 3.1: Abstract……………………………………………………………...… 48 3.2: Introduction………………………………………………………….… 49 3.3: Methods……………………………………………………………….. 53 3.4: Results……………………………………………………………….… 56 3.5: Discussion…………………………………………………………...… 60 Chapter 4: Historical and modern mercury biomagnification patterns in three large North American lakes..………………………………………………………. 78 4.1: Abstract…………………………………………………….………….. 78 4.2: Introduction…………………………………………….……………… 79 4.3: Methods……………………………………………………………….. 81 4.4: Results…………………………………………………………………. 88 4.5: Discussion…………………………………………………………...… 89 Chapter 5: Conclusion……………………………………………………………....106 5.1: Thesis overview……………………………………………………..… 106 5.2: Preservation effects………………………………………………….… 107 5.3: Hg and food webs of the study lakes………………………………..… 109 5.4: Future directions…………………………………………….………… 112 5.5: Summary of key conclusions…………………………………..……… 115 Literature Cited………………………………………………………………..…… 116 Appendix: Museum records for archived fish…………………………………...… 127 vii List of Tables Chapter 2 Table 1. Sensitivities and limits of detection of elements in ICP-MS and ICP-OES.......................................................................................... 35 Table 2. Means and standard deviations of 15N, 13C, and Hg concentrations through time............................................................. 36 Table 3. Mean concentrations in month 0 (control) and month 24 of elements other than Hg.................................................................... 37 Table 4. Preservation effects on fish muscle stable isotope ratios in other studies.............................................................................................. 38 Chapter 3 Table 1. Fish species abbreviations and common names used throughout paper………………………………………………………………. 71 Table 2. General characteristics of the study lakes. ……………………….. 72 Table 3. Sample sizes and standard length ranges of fish in historical and modern datasets…………………………………………………… 73 Table 4. Summary of stable isotope metrics……………………………….. 74 Chapter 4 Table 1. Fish species abbreviations and common names used throughout paper………………………………………………………………. 98 Table 2. General characteristics of the study lakes………………………… 99 Table 3. Sample sizes and standard length ranges of fish in historical and modern datasets…………………………………………………… 100 Table 4. Summary statistics of lake trout Hg monitoring records that were used…………………………………………………………. 101 Appendix…………………………………………………………………………… 121 Table A1. Records of fish used in thesis………………………………….... 121 Table A2. Records of fish analyzed for stable isotopes, but not used in thesis……………………………………………………….… 123 viii List of Figures Chapter 2 Fig. 1. Stable isotope composition of N and C over time……………….… 39 Fig. 2. Elemental composition (as a percentage) of samples over time…… 40 Fig. 3. Muscle 13C composition as a function of C content………………. 41 Fig. 4 Hg concentrations over 12 months..…………………………………42 Fig. 5. Elements whose concentration increased and then decreased over time……………………………………………………………….... 43 Fig. 6. Elements whose concentration rapidly increased in first month and remained relatively stable.…………………………………............. 44 Fig. 7. Elements whose concentration rapidly decreased in first month…... 45 Fig. 8. Per mille change in mean 15N and 13C during preservation in stable isotope studies………………………………………………………46 Fig. 9. Percent change in mean THg concentrations from control (unpreserved) samples over time…………………………………………………...47 Chapter 3 Fig. 1. Timeline of some key events affecting the fish communities of the study lakes………………………………………………………….