Direct and Indirect Impacts of Turbidity and Diet on an African Cichlid Fish
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Living in a haze: Direct and indirect impacts of turbidity and diet on an African cichlid fish Thesis Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Tiffany Lynn Atkinson Graduate Program in Environment and Natural Resources The Ohio State University 2019 Thesis Committee Dr. Suzanne M. Gray, Advisor Dr. Lauren M. Pintor Dr. Roman P. Lanno Dr. Lauren J. Chapman Copyrighted by Tiffany Lynn Atkinson 2019 2 Abstract Worldwide, a major threat to aquatic systems is increased sediment runoff, which can lead to elevated levels of turbidity. In an increasingly variable world, the ability for animals to respond rapidly to environmental disturbance can be critical for survival. Chronic and acute turbidity exposure can have both indirect and direct effects on fish across large and small spatial scales. Indirect impacts include alteration of the sensory environment of fishes (disrupting communications) and shifts in prey availability; while direct impacts include damage to respiratory organs or eliciting physiological compensatory mechanisms that influence fitness- related traits associated with reproduction and survival. I used a combination of field and laboratory studies to examine the effects of elevated turbidity on an African cichlid fish (Pseudocrenilabrus multicolor victoriae). This sexually dimorphic species is widespread across the Nile River basin and is found across extreme environmental gradients (e.g. dissolved oxygen, turbidity). I investigated if within-population variation in diet and male nuptial coloration are associated with turbidity on a microgeographic spatial-scale. Diet was investigated because many cichlid fish depend on dietary carotenoids (red and yellow pigments) for their reproductive displays and other physiological mechanisms associated with health. I found that fish from mostly clear waters ate a higher proportion of plant material and males were more colorful than fish found at more turbid locations. This could indicate that male reproductive traits are plastic across environmental extremes. In the laboratory study, I used a split-brood rearing experiment iii to investigate the effects of turbidity level (high/low) and dietary carotenoid concentration (trace/low) on reproductive traits in P. multicolor. I found that chronic turbidity and carotenoid diets had differential effects on males and females: nuptial coloration and gonadosomatic index were higher in males reared under high turbidity and the trace-carotenoid diet, while exposure to chronic turbidity (but not carotenoid diet) had a negative effect on the overall size of female P. multicolor. This could indicate that some level of stress from chronic turbidity and diet creates an environment where males invest more in immediate reproduction vs. future reproduction and long-term somatic health. It also indicates that the stress from turbidity negatively influenced female size, which is often correlated with fecundity, possibly due to reduced reaction distance and ability to acquire food. I also investigated the effect of acute and chronic turbidity exposure on the swimming performance of P. multicolor. I found that swimming performance was improved by acute turbidity exposure, and chronic turbidity exposure had no effect. This could mean that the aerobic capacity of P. multicolor, under low-to-moderate levels of chronic turbidity, is unaffected possibly due to compensatory adaptations. Additionally, the ability to perform better under acute turbidity exposure may point towards behavioral mechanisms as an attempt to remove themselves from an environmental stressor. This study has helped to emphasize that the impact of turbidity varies due to a number of circumstances such as concentration, duration of exposure, species, and sex. By further investigating the effects of turbidity as a stressor on traits associated with reproduction and survival of a fish found naturally across both extremes, we can further our understanding of the mechanisms that contribute to the persistence of fish facing human-induced environmental changes. iv Acknowledgments I would like to thank the Commissioner of Fisheries Resources Management and Development, Uganda, for permission to export preserved specimens, and the Uganda National Council for Science and Technology (UNCST) for research permission. I would also thank Dr. Lauren Chapman for use of research facilities in Uganda (Lake Nabugabo Research Station); Dr. Dennis Twinomigisha and Ugandan field assistants (Mutebi, Kiberu, Sseygoya, and Geoffrey) for invaluable help whilst in Uganda. A special thanks to Dr. Jessica Cooperstone for help with carotenoid analyses. I would also like to thank B. Tracy, N. Episcopo, R. MacDonald, H. Fried, R. Oldham, T. Hrabak, B. Drohan, N. Steffensmeir, G. Ravary, C. Nieman, B. Williams, J Evans, and K. Dean for assistance with fish rearing, laboratory work, and data entry; the Gray and Pintor lab members for their continued support; and my mother, Theresa Warner, for reminding me to breathe. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE-1343012. Research support provided by state and federal funds appropriated to The Ohio State University, College of Food, Agricultural, and Environmental Sciences, Ohio Agricultural Research and Development Center. Further funding was provided by The Ohio State University Office of International Affairs Academic Enrichment Grant and American Cichlid Association Guy D. Jordan Research Fund. v Vita Education 2016-19 M.S. Environmental and Natural Resources, The Ohio State University 2010-16 B.S. Environmental Science- Water Science, The Ohio State University Research Experience 2016-19 NSF Graduate Research Fellow, The Ohio State University Supervisor- Dr. Suzanne M. Gray 2014-16 Undergraduate Honors Student Researcher, The Ohio State University Supervisor- Dr. Suzanne M. Gray 2014 Research Experience for Undergraduates, Ohio Sea Grant’s Stone Laboratory Supervisor- Dr. Doug Kane Publications Atkinson T., Desrosiers S., Townsend T., and Simon T. P. 2015. Length-weight relationships of the Emerald Shiner (Notropis atherinoides, Rafinesque 1818) in the Western Basin of Lake Erie. Ohio J. Sci. DOI: http://dx.doi.org/10.18061/ojs.v114i2.4719 Fields of Study Major Field: Environment and Natural Resources vi Table of Contents Abstract .......................................................................................................................................... iii Acknowledgments........................................................................................................................... v Vita ................................................................................................................................................. vi List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................. x Chapter 1. ........................................................................................................................................ 1 References ................................................................................................................................... 6 Chapter 2 ......................................................................................................................................... 9 Abstract ....................................................................................................................................... 9 1. Introduction ........................................................................................................................... 10 2. Materials and Methods .......................................................................................................... 17 3. Results ................................................................................................................................... 22 4. Discussion ............................................................................................................................. 25 References ................................................................................................................................. 32 Figures....................................................................................................................................... 41 Chapter 3 ....................................................................................................................................... 45 Abstract ..................................................................................................................................... 45 1. Introduction ........................................................................................................................... 46 2. Materials and Methods .......................................................................................................... 52 3. Results ................................................................................................................................... 59 4. Discussion ............................................................................................................................. 61 References ................................................................................................................................