Exploring the mechanisms that control the success of symbiotic nitrogen fixers across latitude: Temperature, time-lags, and founder effects

Symbiotic nitrogen fixation is the greatest potential input of nitrogen into terrestrial ecosystems. As a result, nitrogen fixation is critical to the functioning of the land carbon sink and its capacity to offset anthropogenic CO2 emissions and climate change. However, our understanding of the controls over nitrogen fixation rates and nitrogen fixing tree abundance is limited, resulting in paradoxes such as the relative absence of nitrogen fixing trees at high latitudes (where nitrogen is most limiting and it seems that nitrogen fixation should be most beneficial) and tropical forest nitrogen saturation, a mechanistically poor representation of nitrogen fixation in terrestrial biosphere models, and incomplete theory for variation in the successional trajectories of nitrogen fixing trees. This dissertation consists of four chapters that examine the drivers of symbiotic nitrogen fixation rates and the abundance of nitrogen fixing trees as they pertain to latitude, climate, and nitrogen fixation strategies. In chapter 1, I develop a method to measure coupled nitrogen fixation and plant carbon exchange in real-time, non-destructively, continuously, and at the whole plant scale. This permits a study of the controls of nitrogen fixation rates over timescales that range from seconds to months. In chapter 2 and 3, I apply the method developed in chapter 1 to determine the temperature response of nitrogen fixation rates and the timescales over which nitrogen fixation is regulated. For chapter 2 and 3, I grew nitrogen fixing tree species of tropical and temperate origin and representing the two types of nitrogen fixing symbioses (rhizobial and actinorhizal) across a 10 °C gradient of growing temperatures. In chapter 2, I show that nitrogen fixation depends on growing temperature and geographic origin and peaks at 30-38 °C, which is 5-13 °C higher than previous estimates based on other nitrogen fixing symbioses and 3-7 °C higher than net photosynthesis. These findings have direct implications for how nitrogen fixation is represented in terrestrial biosphere models and are in direct contrast to terrestrial biosphere model predictions of a decline in tropical nitrogen fixation with warming associated with climate change. In chapter 3, I show that nitrogen fixation takes 1-3 weeks to be down-regulated by 50% following an alleviation of nitrogen limitation, 1-5 weeks to be up-regulated by 50% following the initiation of nitrogen fixation when nitrogen becomes limiting, and up to 4 months for nitrogen fixation to start following a drastic reduction in soil nitrogen supply. Theory says that time-lags in regulating nitrogen fixation start becoming important for plant competition and losses of available nitrogen from ecosystems if they are between 1 day and 1 week. Thus, time-lags on the order of multiple weeks are a significant cost of a facultative nitrogen fixation strategy and resolve the tropical nitrogen forest nitrogen paradox characterized by high losses of available nitrogen at the ecosystem scale in spite of down-regulation of nitrogen fixation at the individual scale. In chapter 4, I show that nitrogen fixing tree abundance is bimodal in all regions of the contiguous United States except the Northeast and that founder effects can explain this pattern and the persistence of nitrogen fixing trees in old forests. Using theory, I show that founder effects are most probable at intermediate soil nitrogen supply, when nitrogen fixers have a high relative capacity to uptake available nitrogen, and when nitrogen fixing trees are facultative in their nitrogen fixation strategy. These chapters provide a new tool for studying nitrogen fixation, critical data for improving terrestrial biosphere models and our understanding of how nitrogen fixation and nitrogen cycling varies across latitude and how it will change with climate change, and new theory for the successional trajectories of nitrogen fixers