The Effect of Temperature on the Ecology, Evolution, and Biogeography of Phytoplankton

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The Effect of Temperature on the Ecology, Evolution, and Biogeography of Phytoplankton THE EFFECT OF TEMPERATURE ON THE ECOLOGY, EVOLUTION, AND BIOGEOGRAPHY OF PHYTOPLANKTON By Mridul Kanianthara Thomas A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of Zoology—Doctor of Philosophy Ecology, Evolutionary Biology and Behavior—Dual Major 2013 ABSTRACT THE EFFECT OF TEMPERATURE ON THE ECOLOGY, EVOLUTION, AND BIOGEOGRAPHY OF PHYTOPLANKTON By Mridul Kanianthara Thomas Temperature is a fundamental driver of biological dynamics, but we do not know how it shapes the physiology and ecology of any community across global temperature gradients. Here I examine the influence of temperature on phytoplankton, which are extremely sensitive to changes in environmental conditions and play a critical role in global food webs and biogeochemical cycles. I address how global variation in temperature regimes has shaped distributions of phytoplankton temperature traits, identifying patterns of adaptation as well as differences in how major functional groups respond to environmental temperature gradients. I also show that due to the asymmetric cost of exceeding the optimal temperature and the traits of tropical species, ocean warming this century may drive a reduction in the diversity of tropical phytoplankton communities in the absence of evolutionary adaptation. Tropical phytoplankton species may persist, however, by poleward migration, bringing them into competition with temperate species. Our study of the temperature traits of an invasive cyanobacterium supports the idea that rising temperatures will increase the probability of invasion by tropical and subtropical species into temperate environments. Predicting these invasions, however, is a challenge that requires us to model the phytoplankton community dynamics in complex natural environments. This will require a mechanistic understanding of how temperature interacts with important resources such as nutrients and light to influence growth. To address this, I have developed and tested a model describing how temperature and nutrients interact to affect growth rates. Our experimental tests confirm a novel prediction: that optimum temperature for growth is a saturating function of nutrient concentration. Together, this work forms a foundation from which we can build predictive models of how environmental warming will affect population and community dynamics across broad spatial scales. Copyright by MRIDUL KANIANTHARA THOMAS 2013 Dedicated to my parents and my wife. v ACKNOWLEDGEMENTS As with any effort stretching over the better part of a decade, this work could not have been done without a great deal of help. I’m indebted to Elena Litchman, my advisor, for giving me the opportunity to pursue a career as an ecologist, free rein to pursue ideas I found interesting, and for guidance, criticism, and funding along the way. Chris Klausmeier, Colin Kremer, and Kyle Edwards taught me far more about ecological theory and analytical techniques than I could possibly have learned on my own; my thanks can’t do justice to their patience and generosity with their time. Gary Mittelbach and Jen Lau critiqued my (initially extremely naïve) ideas and have shaped the way I think about ecology and evolution. I’m very grateful to Pam Woodruff and Ally Hutchens for helping tremendously with my laboratory work over the years, and tolerating my (hopefully) occasional fumbles in that regard. The KBS academic community – faculty, postdocs, and graduate students – all made me a far better scientist by forcing me to defend and refine my ideas on a regular basis. And my experimental work could not have been done without the assistance of a number of undergraduates who worked in our lab: Caitlin Ryan, Alexandra David, Marilyn Gould, and Lydia Auner. vi TABLE OF CONTENTS LIST OF TABLES .....................................................................................................ix LIST OF FIGURES ...................................................................................................x CHAPTER 1 ..............................................................................................................1 INTRODUCTION .....................................................................................................1 LITERATURE CITED ..................................................................................5 CHAPTER 2 A GLOBAL PATTERN OF THERMAL ADAPTATION IN MARINE PHYTOPLANKTON……………… .........................................................................7 ABSTRACT ...................................................................................................7 INTRODUCTION .........................................................................................7 METHODS ....................................................................................................8 RESULTS AND DISCUSSION ....................................................................9 LITERATURE CITED ..................................................................................20 CHAPTER 3 ENVIRONMENT AND EVOLUTIONARY HISTORY DETERMINE THE GLOBAL BIOGEOGRAPHY OF PHYTOPLANKTON TEMPERATURE TRAITS......................................................................................................................24 ABSTRACT ...................................................................................................24 INTRODUCTION .........................................................................................24 METHODS ....................................................................................................29 Model comparison and parameter estimation ......................................30 RESULTS ......................................................................................................32 1. Optimum temperature for growth ....................................................32 2. Maximum persistence temperature (Tmax) .....................................34 3. Minimum persistence temperature (Tmin) ......................................34 4. Temperature niche width .................................................................38 5. Maximum growth rate......................................................................39 DISCUSSION ................................................................................................40 LITERATURE CITED ..................................................................................48 CHAPTER 4 INTERACTIVE EFFECTS OF TEMPERATURE, NITROGEN AVAILABILITY, AND TOXICITY ON THE GROWTH OF INVASIVE AND NATIVE CYANOBACTERIA .................................................................................................54 ABSTRACT ...................................................................................................54 INTRODUCTION .........................................................................................55 METHODS ....................................................................................................59 Strains used ..........................................................................................59 vii Culture conditions ................................................................................60 Experiment ...........................................................................................60 Calculation of specific growth rate .....................................................61 Secondary analysis of published data ..................................................62 Calculation of optimum temperature for growth .................................62 Comparison of temperature response of strains with different toxicities ...............................................................................................63 RESULTS ......................................................................................................64 Growth in N-replete medium ...............................................................64 Effect of N-deprivation at different temperatures ................................64 Toxicity ................................................................................................70 DISCUSSION ................................................................................................70 Climate change and C. raciborskii.......................................................73 Adaptation to environmental conditions ..............................................75 Effects of N-deficiency ........................................................................75 Toxicity ................................................................................................76 LITERATURE CITED ..................................................................................78 CHAPTER 5 INTERACTIVE EFFECTS OF TEMPERATURE AND NUTRIENT CONCENTRATION ON THE GROWTH RATES OF PHYTOPLANKTON .........84 ABSTRACT ...................................................................................................84 INTRODUCTION .........................................................................................84 MODEL .........................................................................................................87 Effect of temperature on growth rate ...................................................87 Effect of nutrients on growth rate ........................................................88 Effect of temperature-nutrient interactions on growth rate ..................88 METHODS ....................................................................................................90
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