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Microcystin in Ugandan lakes: Production dynamics, accumulation in fish, and risk evaluation by Amanda Elizabeth Poste A thesis presented to the University of Waterloo in fulfillment of the thesis requirement for the degree of Doctor of Philosophy in Biology Waterloo, Ontario, Canada, 2010 ©Amanda Elizabeth Poste 2010 AUTHOR'S DECLARATION I hereby declare that I am the sole author of this thesis. This is a true copy of the thesis, including any required final revisions, as accepted by my examiners. I understand that my thesis may be made electronically available to the public. ii Abstract Eutrophication of freshwater lakes has led to an increase in the occurrence of harmful cyanobacterial blooms, and it is expected that a warming climate will further exacerbate the frequency and duration of such blooms. Microcystin is a cyanobacterial hepatotoxin that is found worldwide, and poses a serious threat to the ecological communities in which it is found as well as to those who use these waters for drinking, recreation, or as a food source. Although microcystin is known to accumulate in fish and other aquatic biota, the prevalence of microcystin in fish tissue and the human health risks posed by microcystin exposure through fish consumption remain poorly resolved. Very few studies have quantified microcystin (a broadly present cyanotoxin) in water from East African lakes, despite the large human and animal populations that rely on these lakes for both water and food, and to date there is very little information available on the accumulation of microcystin in fish from these lakes. A comprehensive set of water and fish samples was collected on a monthly basis between September 2008 and February 2009 from several lakes in Uganda. The study sites included two embayments in northern Lake Victoria (Murchison Bay and Napoleon Gulf), Lake Edward, Lake George, Lake Mburo, and the crater lakes Saka and Nkuruba. The large lakes sampled all support substantial commercially important fisheries, while the smaller lakes support subsistence fisheries that provide a critically important source of protein and income for riparian communities. Microcystin concentrations in water were determined in addition to chlorophyll and nutrient concentrations, phytoplankton community composition, mixing dynamics and light conditions. At all study sites except Lake Nkuruba, microcystin concentrations in water regularly exceeded the WHO guideline for microcystin in drinking water of 1.0 µg/L. Microcystis spp. emerged as the cyanobacterial taxa that is primarily responsible for microcystin production in these lakes, and as such, microcystin concentrations were closely linked to environmental factors that favour the development of high Microcystis biomass, including high nutrient concentrations, as well as shallow mixing depth which acts to increase mean mixed layer light intensity. Because of the importance of understanding the underlying food web when considering the accumulation and trophic transfer of a compound, stable carbon and nitrogen isotope analysis was used to characterize the food webs at the previously mentioned Ugandan study sites as well as in the East African great lake Albert. Omnivory was found to be common at all study sites, and based on δ13C values, the food webs in these lakes were strongly based on pelagic primary production, with no strong evidence of iii substantial benthic contribution to these food webs, likely as a result of reduced benthic primary productivity in these generally low-transparency eutrophic lakes. The distribution and trophic transfer of mercury was also characterized in the Ugandan study lakes (including Lake Albert) in order to provide a contrast for the trophic transfer of microcystin in the same lakes. Furthermore, relatively little is known about the behaviour of mercury in tropical hypereutrophic lakes, and the study sites included in the current study provided an opportunity for the exploration of this topic. Consistent biomagnification of mercury was observed at all study sites; however, mercury concentrations in fish were generally low, and would not be expected to pose a risk to consumers. Mercury dynamics were strongly linked to lake trophic status, with biomagnification rates significantly lower at the hypereutrophic study sites than at the mesotrophic and eutrophic study sites. I found evidence that growth and possibly biomass dilution can reduce mercury concentrations at the base of the food web, while growth dilution of mercury at consumer trophic levels might effectively reduce the biomagnification rate of mercury in these hypereutrophic lakes. Microcystin was prevalent in fish muscle tissue from all study sites and at all trophic levels. In contrast to mercury, for which consistent biomagnification was observed, neither biomagnification nor biodilution was observed for microcystin; and concentrations were relatively consistent throughout the fish food web, including in top predators, indicating that efficient trophic transfer of microcystin is occurring in these lakes. Microcystin concentrations in fish from several study sites followed seasonal trends that were similar to those observed for microcystin concentrations in water at these sites, suggesting that fish can rapidly respond to changes in microcystin concentrations in water through accumulation and depuration of this toxin. Microcystin concentrations in water and fish from all Ugandan study sites (including Lake Albert) in addition to data from two temperate eutrophic embayments (Maumee Bay in Lake Erie, and the Bay of Quinte in Lake Ontario) were compiled and used to estimate potential microcystin exposure to human consumers of both water and fish from these study sites. Microcystin was pervasive in water and fish from both the tropical and temperate study sites. Also, these results establish that fish consumption can be an important and even dominant source of microcystin to humans, and can cause consumers to exceed recommended total daily intake guidelines for microcystin. These results highlight the need to consider potential exposure to microcystin through fish consumption in addition to water consumption in order to adequately assess human exposure and risk. iv Acknowledgements To Drs. Stephanie Guildford, Bob Hecky and Bill Taylor, my co-supervisors, thank you for your support and guidance throughout the past five years. Bob and Stephanie, you were always generous with your time, insight, funding, and enthusiasm; and you were excellent hosts in Duluth. Bill, you have looked out for me over the past few years, and have always made sure to make me feel welcome in your lab. To my committee members Drs. Kirsten Müller, Sherry Schiff and Derek Muir, thank you for your valuable input to this thesis. Derek, you have been especially supportive of my work through your intellectual input, and by so generously allowing me to run my mercury samples in your lab. The International Development Research Council provided an IDRC Doctoral Research Award, which supported my six-month sampling trip to Uganda. Great Lakes Fisheries Commission and National Instututes of Health grants to S. Guildford supported work on the Laurentian Great Lakes, while National Science and Engineering Research Council Post-Graduate Scholarships together with University of Waterloo funding (both scholarships and teaching assistant positions) supported me financially while in Canada. To Dr. John Balirwa and the staff of NaFIRRI, thank you for making me feel at home in Jinja and for giving me office and lab space. In particular I would like to thank Dr. William Okello, who taught me a great deal about cyanotoxins in Ugandan lakes, made my 2007 Ugandan field sampling possible, and was great company during field and lab work. Also, to Dr. Dismas Mbabazi, thank you for your friendship and for teaching me about the fish of Uganda. To Drs. Lauren and Colin Chapman, as well as the Kibale Forest Field Station Staff (Patrick Aria, Dennis Twinomugisha, and Emmanuel Amooti), thank you for letting me join you on sampling expeditions to Lakes Saka and Nkuruba, for helping me set fish nets and traps, and for your hospitality at the field station. To Greg Lawson, who ran my water THg samples, thank you for teaching me to use the DMA-80, and for finding time to discuss my results. To Xiaowa Wang, Jane Kirk and Christina Skrypka, thank you for arranging time for me on the DMA-80 and for providing valuable technical guidance. To the Lake Erie Centre, and Tom Bridgeman, Carol Stepien and Jona Scarbro, thank you for making my work on Maumee Bay. To Satyendra Bhavsar, Patrick Kocovsky, and Colin Lake, thank you for providing me with fish from the western basin of Lake Erie and the Bay of Quinte. To Juli Dyble, thank you for carrying out microcystin analysis on fish, and for helping me to interpret the results; and to John Berry, thank you for hosting me in Miami and for teaching me the ins and outs of ELISA. v This work would not have been possible without the help and support of numerous fellow graduate students and field and lab technicians. For work on Maumee Bay and the Bay of Quinte, Sarah Yakobowski and Aline Chhun were partners in planning sampling trips, while Adam Houben was a great help in the field. Ann Balasubramaniam, Tomson Hecky, Zing-Ying Ho, Justin Lorentz and Duša Vukosavljević also helped in both the field and the lab. To Zing-Ying in particular, you were always cheerful and hard working, even when the tasks weren’t the most exciting. Thanks to Thomas Pevan, who helped me extensively with water chemistry and ELISA analyses in Duluth; Dave Depew and Joel Harrison, who ran CHN samples; and Bill Mark, who ran stable isotope samples and was always willing to answer my questions. From NaFIRRI, I would like to thank Henry Ocaya, who carried out fieldwork with me on Lake Ablert; Ghandi Pabire, who identified benthic macroinvertebrates; Musana Issa, a coxswain with whom I spent many early mornings on Napoleon Gulf; and Rogers Kalyowa, who drove me all over Uganda each month. Special thanks to Alex Aguzu, who carried out phytoplankton counts, and spent six months of long days (and often long nights) in the field and lab with me in Uganda, and who was always a pleasure to work with.

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