The Ecophysiology of Photosynthetic Heat Tolerances in Tropical Plants

Temperature governs several biological processes from molecular to macroecological scales. Underlying many ecological processes is the assumption that fitness is constrained by the physiological limits of species’ metabolic function. The thermal limits of metabolic function, termed thermal tolerances, are often assumed to directly translate into the environmental conditions that define species’ abiotic thermal niches. When species exceed their physiological thermal tolerances, it is expected to negatively impact fitness, and may therefore provide a basis for understanding the environmental constraints on species distributions. Given the rising temperatures caused by climate change, heat tolerances are of particular interest for understanding these constraints. Heat damage in plants has the potential to influence growth rates, which are tied to fitness and contribute to ecosystems services like carbon sequestration that modulate climate change. Photosynthesis is a temperature-sensitive metabolic process, and photosynthetic heat tolerances can be readily assessed, but provide only incomplete information for understanding whole-plant fitness. Understanding the effect of thermal damage on plant growth is necessary if heat tolerances are to predict species thermal niches, their geographic distributions, or their responses to climate change. This dissertation investigates the ecophysiology of heat tolerances in order to advance their use in linking ecological patterns to physiological processes. In the first chapter we provide an introduction to heat tolerances and a review of existing heat tolerance literature. In this review, we call attention to the different sources of methodological variation likely to bias estimates of plant heat tolerances. Using the newly assembled database of heat tolerances, we illustrate current the methodological biases that may prevent heat tolerances from being integrate into ecological contexts. We also discuss how environmental conditions like a) growth temperature, b) drought, c) light, d) salinity, and e) ontogenetic stage can cause variation in estimates of heat tolerance. Finally, we propose a standardized terminology to facilitate interpretation of heat tolerance data among studies. One issue limiting the use of heat tolerances to understand species distributions is mixed support for the hypothesis that hotter climates select for higher heat tolerances. Furthermore, the limited heat tolerance data that exist indicate some taxonomic groups have distinct ranges of heat tolerances. In the second chapter we hypothesized that phylogenetic structure may help to explain variation in heat tolerances, resolve the conflicting effects that climate has been observed to have on heat tolerances, and advance the use of heat tolerances in broader ecological contexts. To address our hypothesis, we measured the heat tolerances for 123 species of ferns, gymnosperms, magnoliids, monocots, and eudicots grown in a common climate at Fairchild Tropical Botanic Garden and the John C. Gifford Arboretum in Miami, FL USA. Phylogenetic analysis using Blomberg’s K indicated that species’ heat tolerances are not phylogenetically conserved, but data from the five groups we studied suggest there may be some evolutionary constraints on plant heat tolerances at coarse phylogenetic resolutions that are potentially related to leaf thermoregulation. Phylogenetic independent contrasts of heat tolerance and climatic data for 102 species revealed limited support for the hypothesis that climate can predict species heat tolerances. We also re-analyzed the effect of climate on heat tolerances using a subset of our study species that were most unlikely to experience heat tolerance down-regulation, which confirmed the inability of climate to predict species heat tolerances. We conclude that there are weak phylogenetic and climatic constraints on the heat tolerances of plants. In the third chapter, we attempt to develop a mechanistic explanation for the variation in heat tolerance among species. Given that plants exhibit unique thermoregulatory traits that influence leaf temperatures, and that leaf temperatures can be decoupled from ambient air temperatures, we hypothesized that photosynthetic heat tolerances are adapted to extreme leaf temperature as opposed to coarse climatic variables. We measured thermoregulatory traits, maximum leaf temperatures and two different metrics of photosynthetic heat tolerances for 19 plant species growing at Fairchild Tropical Botanic Garden (Coral Gables, FL, USA). The first metric of heat tolerance is termed Tcrit and is defined as the temperature that causes an initial decrease in the quantum yield of photosynthesis. The second metric of heat is termed T50 and is defined as the temperature that cause as a 50% reduction in the quantum yield of photosynthesis. The thermoregulatory traits measured at the Garden were used to parameterize a leaf energy balance model and predict maximum in situ leaf temperatures across the geographic distributions of 13 species. The maximum observed leaf temperatures and maximum predicted in situ leaf temperatures were positively correlated with only heat tolerances. The breadth of species’ thermal safety margins (the difference between heat tolerance and leaf temperature for T50) was negatively correlated with T50. Our results provide observational and theoretical support for the hypothesis that photosynthetic heat tolerances are adapted to extreme leaf temperatures, but refute the assumption that species with higher PHTs are less susceptible to thermal damage. Tree growth is an important predictor of tree survival and component of the global carbon sink that is potentially negatively influenced by thermal damage. In the fourth chapter, we investigate the ability of heat tolerances to predict annual growth for eight tropical tree species. More specifically, we test the hypotheses that 1) species with higher heat tolerances are more likely to experience decelerating growth rates across multiple years; and 2) thermal safety margins are capable of predicting species’ annual growth rates. Our results suggest that only species with a combination of high leaf temperatures and low heat tolerances are expected to experience thermal damage, but that thermal damage is unlikely drive changes in species’ growth. Instead of heat tolerances, our results point to optimal temperatures for photosynthesis, not respiration, as a promising physiological mechanism explaining species growth rates. Nevertheless, Tcrit may provide a limited ability to explain growth deceleration when photosynthesis ceases, while and T50 may act as a thermal constraint on leaf size