Analysis and prediction of plant functional traits in contrasting environments: information for next-generation ecosystem models By Henrique Furstenau Togashi Supervised by I. Colin Prentice Owen K. Atkin Ian J. Wright Suzanne M. Prober Craig Macfarlane Michael J. Liddell A thesis submitted to Macquarie University for the degree of Doctor of Philosophy Faculty of Science and Engineering Department of Biological sciences February 2016 ii © Henrique Furstenau Togashi, 2016. iii I certify that the work in this thesis has not previously been submitted for a degree nor has it been submitted as part of requirements for a degree to any other university or institution other than Macquarie University. I also certify that the thesis is an original piece of research and it has been written by me. Any help and assistance that I have received in my research work and the preparation of the thesis itself have been appropriately acknowledged. In addition, I certify that all information sources and literature used are indicated in the thesis. Henrique Furstenau Togashi Acknowledgements I thank Macquarie University for supporting me through the International Macquarie University Research Excellence Scholarship (iMQRES) during the past three and a half years. I also extend my gratitude to the Terrestrial Ecosystem Research Net- work (TERN) organisation and to the Ecosystem Modelling and Scaling Infrastructure (eMAST) facility for financial support and for funding my fieldwork in Australia. It has been a great opportunity to work with Professor Colin Prentice, my primary supervisor. Colin is a very influential scientist in Earth System Modelling, and a great supervisor. He was always available when I needed help, and always encouraged me to work towards novel science. His ideas and guidance led me to expand my understanding of science greatly. Colin's network permitted me to work with and learn from leading scientists in plant physiology and biogeography. His prestige and hard work were essential to obtain grants that allowed me to go on fascinating campaigns to collect plant data. I am so grateful to Colin, and I can't think of anyone who could be a better mentor, offering so many amazing opportunities for a student to learn. I thank Professor Owen Atkin, my associate supervisor and an internationally recog- nised scientist, who taught me a great deal about ecophysiology and leaf gas exchange methods. He was as important as Colin in obtaining the grants that made my fieldwork possible. He was also present in the early campaigns, making sure we were successful in collecting the data. His positive criticism on part of my work was crucial for my development as a scientist. Owen also organised a TERN workshop in which I had the great opportunity to expand my network by meeting the Australian leading scientists iv v in the area. My other associate supervisors also had a very important role in my progress. I am grateful to Dr Ian Wright for many discussions about my results. I thank Dr Suzanne Prober and Dr Craig Macfarlane, who provided scientific and field support to my work at the Great Western Woodlands; and Professor Mike Liddell during my work at Robson Creek. Thanks to Dr Brad Evans who was my employer over last year at eMAST. He shared his knowledge in obtaining and creating products from gridded data, motivated me to learn the python programming language, how to create spatial products following international standards, along with how to manage complex databases. His input was fundamental to my learning in a wide variety of extremely useful scientific skills. I am thankful to my lab colleagues, Guangqi Li, Dr Rhys Whitley, Anna Ukkola, Dr Ines Hessler, Dr Wang Han, Ian Marang, Shuang Zhou, Ning Dong, Yasmin Hageer, Douglas Kelley, Annika Herbert, Dr Kevin Willis, and Farzana Raihan. They helped me on the most diverse kinds of tasks including science discussions, fieldwork, writing grant applications, and setting up the required computer tools to process and analyse data. I am grateful to Dr Keith Bloomfield for the discussions about ecophysiology, for managing the field campaigns in Australia, for reviewing part of my work, and for his hospitality in my trips to Canberra. Dr Lasantha Weerasinghe contributed in early stages of the Australian fieldwork and also helped me understand more about ecophysiology and leaf gas exchange. Thanks to Professor David Ellsworth for his comments on some of my results, for inviting me to participate in some of his research group activities, and for answering my questions of plant physiology. I would like to thank Professor Tomas Domingues, Professor Maurizio Mencuccini, Professor Santi Sabate, Dr Lucas Cernusak, Dr Sean Gleason and Dr Daniel Falster for their scientific input on, and giving ideas, about my data. I also recognise scientific contribution in part of my work from Professor Jon Lloyd, Professor Derek Eamus, Professor David Forrester, Dr Paul Drake, Dr Paul Feikema and Dr Kim Brooksbank. I acknowledge support on fieldwork by Jack Egerton, Lingling Zhu, Danielle Creek, vi Acknowledgements Desmond Ng, Aurore Penillard, Lucy Hayes, Jinlong Zhang, Professor Sandy Harrison, Professor Jian Ni (funds and network), and Dr Marina Scalon. Dr Matt Bradford contributed fundamental data as well as identified all tree species I collected in Robson Creek. My thanks to Stephanie McCaffery for supervision in the digestion of leaves for nitrogen and phosphorus analysis; and to Professor Brian Atwell, Muhammad Masood and Ray Duell for all laboratory support. Diego Barneche, thanks for the great help with R scripts. I want to thank the entire Biological Sciences Department of Macquarie Univer- sity including, but not restricted to, Teresa Potalivo, Marie Howitt, Laura McMillan, Professor Marie Herberstein, Samantha Newton, and especially Veronica Peralta who booked my student trips and resolved most of my paperwork. Thanks also to Jane Yang and Ana Borba from the Higher Degree Research team at Macquarie University. Last, but not least, I have to mention my family that always accepted all my decisions, particularly my choice of living overseas for so long. Gabriela, Rafael, Akira, Erica, Vera, and Yoko, I would not have finished this thesis without your support. Thank you. Abstract Three empirical plant-trait studies are presented, based on new field data plus extensive data analysis. All aim to provide information to improve the basis of dynamic global vegetation models (DGVMs), by exploring neglected ecophysiological processes. The first study investigates a key model parameter, the leaf area (LA) to cross- sectional sapwood-area (SA) ratio, in Australian evergreen woody plants. It confirms the pipe model, which states that SA at any point should scale isometrically with LA distal to that point. But although the LA:SA ratio is reported to vary with hydro- climate, aridity determined only upper and lower bounds of LA:SA. Great variation among species in similar environments exists and may reflect variation in stem hy- draulics. The second study refutes the common model assumption that photosynthetic traits of evergreen plants are fixed in time. If it were true, carboxylation capacity (Vcmax) should increase with temperature following Rubisco kinetics. The study employs a theoretical framework to predict, instead, that Vcmax should acclimate to temperature: increasing, but less steeply. Repeat sampling of plants in the semi-arid Great West- ern Woodlands, during the warm and cool seasons, revealed that Vcmax (and other photosynthetic parameters) show thermal acclimation as predicted. The third study focuses on tropical rainforests in Australia and China, occupying a relatively narrow range of climates, to examine the association of plant functional traits (including growth traits such as maximum height as well as field-measured photo- synthetic traits) with species' successional `roles'. Consistent relationships were found, vii viii Abstract providing key information for modelling forest dynamics. Each study tackles an aspect of DGVMs that so far has involved simplifying as- sumptions, such as assigning fixed trait values to functional types without considering variability across environments, seasons, and species. To take account of such varia- tion, DGVM development will require targeted empirical studies like those presented here. Contents Acknowledgements iv Abstract vii List of Figures xiv List of Tables xvi 1 Introduction1 1.1 Impacts of vegetation and human activity on climate . .1 1.1.1 Human activity and alterations in climate and the global carbon cycle . .1 1.1.2 State of the art in land-surface and vegetation modelling . .4 1.1.3 New opportunities for Dynamic Global Vegetation Models . .6 1.2 Plant Functional Types and forest dynamics . .7 1.3 Physiological basis of photosynthesis described by models . .9 1.3.1 The Farquhar model and Fick's law . .9 1.3.2 The evolutionary attractor framework . 13 1.3.3 The least-cost theory and the trade-offs of Vmax, ci:ca, leaf N and the Huber value . 14 1.3.4 The coordination hypothesis . 18 1.3.5 Acclimated responses, least-cost, coordination and PFTs . 19 ix x Contents 1.4 Fieldwork context . 20 1.5 Thesis approach . 22 1.6 Candidate's role . 26 Glossary of terms . 27 1.7 References . 29 2 Morphological and moisture availability controls of the leaf area-to- sapwood area ratio: analysis of measurements on Australian trees 43 2.1 Abstract . 44 2.2 Introduction . 44 2.3 Methods . 45 2.3.1 Measurements and data synthesis . 45 2.3.2 Climate data . 45 2.3.4 Data analysis . 46 2.4 Results . 46 2.4.1 Branch to trunk allometry . 46 2.4.2 Leaf area-to-sapwood area ratio and tree height . 47 2.4.3 Relationship of LA:SA to climatic moisture . 47 2.4.4 Relationship of LA:SA to Ks and climatic moisture . 48 2.5 Discussion . 48 2.5.1 LA to SA allometry in branches and whole trees .