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Thesis with Everything The Pennsylvania State University The Graduate School Department of Geosciences MOLECULAR AND ISOTOPIC INDICATORS OF CANOPY CLOSURE IN ANCIENT FORESTS AND THE EFFECTS OF ENVIRONMENTAL GRADIENTS ON LEAF ALKANE EXPRESSION A Dissertation in Geosciences and Biogeochemistry by Heather V. Graham © 2014 Heather V. Graham Submitted in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy August 2014 The dissertation of Heather V. Graham was reviewed and approved* by the following: Katherine H. Freeman Professor of Geosciences Dissertation Advisor Co-Chair of Committee Lee R. Kump Professor of Geosciences Co-Chair of Committee Peter D. Wilf Professor of Geosciences Mark E. Patzkowsky Associate Professor of Geosciences Erica A.H. Smithwick Associate Professor Ecology Outside Committee Member Scott L. Wing Curator of Paleobotany, Smithsonian Institution Special Member Chris J. Marone Professor of Geosciences Associate for Graduate Programs and Research in Geosciences *Signatures are on file in the Graduate School ii ABSTRACT Dense forests with closed canopies are of enormous climatic and ecological significance. Three-dimensional forest structure affects surface albedo, atmospheric circulation, hydrologic cycling, soil stability, and the carbon cycle, both on the local and global scale. Increasingly, dense canopy forests are recognized for their role in plant and animal evolution and provide a great variety of microhabitats into which much of the diversity of animal and plant life has specialized. The geologic history of three dimensional forest structure is poorly known, however, because fossil assemblages seldom reflect tree spacing, size, or branching and adaptations specific to closed-canopy forests – such as large, fleshy fruits or branchless boles – rarely preserve. The best preserved and most abundant plant fossils are leaves and leaf fragments, however leaf morphology alone does not indicate canopy conditions. This study focuses on leaf biochemical signatures that have potential to record light environment, preserve in geologic archives, and ultimately serve as proxies of canopy density. Dense, closed-canopy forests are defined by strong vertical light and humidity gradients, and a pronounced decrease in photosynthetic rate in the understory. This rate 13 difference results in an enrichment in the carbon isotope composition of leaves (δ Cleaf) at the top of the canopy relative to the lower levels. Our study found that leaves from a 13 deeply-shaded closed-canopy forest in Panama had a ~10‰ vertical range in δ Cleaf values, vertically, while leaves from a seasonal canopied forest in Maryland expressed 13 only a ~6‰ range. A Monte Carlo model that resampled δ Cleaf values indicated that iii canopy closure could be identified by isotopic range from a relatively small (~50) number 13 of leaves. Based on this result, we used δ Cleaf range as a diagnostic feature of canopy 13 coverage and measured δ Cleaf values of fossil leaves to identify canopy density characteristics of three ancient forests. Our results confirm the earliest closed-canopy Neotropical forest in a Paleocene fossil assemblage and identified open canopy features in a Cretaceous fossil assemblage and a forest edge in another Paleocene assemblage. Identifying canopy closure in fossil leaves by analogy by isotopic leaf features observed in modern plants assumes that patterns of photosynthetic carbon isotope fractionation (∆leaf) are the same in ancient plants and their extant relatives. ∆leaf values calculated for modern leaves had a wide range of values from canopy to understory. ∆leaf values calculated from fossil leaf data indicated that the majority of leaves in the assemblages were from the upper canopy. A similar analysis of n-alkanes from modern 13 found that modern leaves express a wide range of δ Clipid values, in correlation with 13 humidity, canopy height, and irradiance. δ Clipid values from fossil leaves had smaller ranges than modern relatives but a mixing model that used the relative abundance of leaves 13 in the assemblage and the fossil δ Clipid data closely reproduced the chain-length 13 distribution and δ Clipid of alkanes from bulks sediments from the fossil assemblage. Calculated fractionation during lipid synthesis (εlipid) in fossil leaves was less negative than modern leaf values and may reflect drier climates or the bias in fossil leaf assemblages toward upper canopy leaves. iv The amount of n-alkanes made by a leaf is greater in the understory than it is in the 13 canopy. Understory leaves also have more depleted δ Clipid values. Alkanes extracted 13 from fossil leaves in the closed-canopy assemblage also exhibited depleted δ Clipid values in leaves with higher alkane content. An analysis of the published literature found leaf higher angiosperms produce greater concentrations of leaf alkanes. The systematic increase in alkane production as well as the higher alkane amounts in understory leaves may be related to the enhanced fungal resistance proffered by alkanes that would be necessary in humid understories. Increased alkane production may then also be related to shade tolerance and early adaptation by higher angiosperms to closed-canopy conditions. v TABLE OF CONTENTS LIST OF FIGURES…………………………………………………………………….. x LIST OF TABLES……………………………………………………………………. xiv ACKNOWLEDGEMENTS………………………………………………...………...xvii EPIGRAPH……………….………………………………………………...……….....xix Chapter 1. Introduction................................................................................................ 1 1.1. Introduction.......................................................................................................... 1 1.2. Climatic feedback in closed-canopy forests .......................................................... 2 1.3. Reconstruction of ancient canopied forests from fossils........................................ 2 1.4. The origin and evolution of the closed-canopy forest in the Neotropics ................ 3 1.5. Biochemical features of canopy closure: The canopy effect.................................. 4 1.6. Isotopic reconstruction of ancient ecosystems....................................................... 6 1.7. The advantages of plant-specific biomarkers in ecosystem reconstruction ............ 7 1.8. Ecophysiology of leaf alkane production.............................................................. 8 1.9. Factors affecting preservation of biomarkers ........................................................ 9 1.10. Factors affecting organic matter preservation in leaf fossils.............................. 10 1.11. Isotopic notation and calculation of isotope fractionation.................................. 11 1.12. Study objectives and chapter outlines ............................................................... 13 1.13. Publications arising from this dissertation......................................................... 15 1.14. References........................................................................................................ 17 Chapter 2. Isotopic characteristics of canopies in simulated leaf assemblages ........ 27 2.1. Abstract.............................................................................................................. 27 2.2. Introduction........................................................................................................ 28 2.3. Methods ............................................................................................................. 33 2.3.1. Collection sites ........................................................................................... 33 2.3.2. Sampling methods and environmental measurements............................. 34 2.3.3. Isotopic analysis methods.......................................................................... 36 2.3.4. Flux and biomass....................................................................................... 38 2.3.5. Bootstrap analysis...................................................................................... 39 2.4. Results ............................................................................................................... 41 2.4.1. Light and height measurements................................................................ 41 2.4.2. Leaf carbon isotope data ........................................................................... 41 2.5. Discussion.......................................................................................................... 42 2.5.1. Light properties and the δ13C canopy effect at San Lorenzo .................. 42 2.5.2. Canopy isotope gradients in biomass and litter flux ................................ 44 vi 2.5.3. Resampling model outcomes ........................................................................ 45 2.5.4. From leaves to soil organic carbon .............................................................. 50 2.6. Conclusions ............................................................................................................ 51 2.7. Figures .................................................................................................................... 53 2.8. References .............................................................................................................. 61 Chapter 3. Biogeochemical confirmation of the first closed-canopy Neotropical forest in the fossil record: A novel application of isotopic methods ........................... 70 3.1. Abstract .................................................................................................................
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