Functional and Floristic Dynamics of Amazonian Forests Adriane Esquivel Muelbert Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Geography September 2016 ii iii The candidate confirms that the work submitted is her own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. Chapter 3 Esquivel-Muelbert, A., Baker, T. R., Dexter, K. G., Lewis, S. L., ter Steege, H., Lopez-Gonzalez, G., Monteagudo Mendoza, A., Brienen, R., Feldpausch, T. R., Pitman, N., Alonso, A., Van Der Heijden, G., Peña-Claros, M., Ahuite, M., Alexiaides, M., Álvarez Dávila, E., Murakami, A. A., Arroyo, L., Aulestia, M., Balslev, H., Barroso, J., Boot, R., Cano, A., Chama Moscoso, V., Comiskey, J. A., Cornejo, F., Dallmeier, F., Daly, D. C., Dávila, N., Duivenvoorden, J. F., Duque Montoya, A. J., Erwin, T., Di Fiore, A., Fredericksen, T., Fuentes, A., García- Villacorta, R., Gonzales, T., Guevara Andino, J. E., Honorio Coronado, E. N., Huamantupa-Chuquimaco, I., Killeen, T. J., Malhi, Y., Mendoza, C., Mogollón, H., Jørgensen, P. M., Montero, J. C., Mostacedo, B., Nauray, W., Neill, D., Vargas, P. N., Palacios, S., Palacios Cuenca, W., Pallqui Camacho, N. C., Peacock, J., Phillips, J. F., Pickavance, G., Quesada, C. A., Ramírez-Angulo, H., Restrepo, Z., Reynel Rodriguez, C., Paredes, M. R., Sierra, R., Silveira, M., Stevenson, P., Stropp, J., Terborgh, J., Tirado, M., Toledo, M., Torres-Lezama, A., Umaña, M. N., Urrego, L. E., Vasquez Martinez, R., Gamarra, L. V., Vela, C. I. A., Vilanova Torre, E., Vos, V., von Hildebrand, P., Vriesendorp, C., Wang, O., Young, K. R., Zartman, C. E. & Phillips, O. L. 2016. Seasonal drought limits tree species across the Neotropics. Ecography AEM, OLP, TRB, KGD, HtS and SLL design the study; all authors contributed to data collection and/or data management; AEM analysed the data and wrote the paper Chapter 4 Esquivel-Muelbert, A., Galbraith, D., Dexter, K. G., Baker, T. R., Lewis, S. L., Da Costa, A. C. L., Meir, P., Nepstad, D., Rowland, L. & Phillips, O. L. in review in Journal of Ecology - Biogeographic distributions predict drought tolerances of Neotropical tree genera. AEM, OLP, DG, KGD, TRB and SLL designed the study; ACLDC, PM, DN, LR collaborated with experimental data, AEM analysed the data and wrote the paper. Chapter 5 In preparation. AEM, OLP, KGD, TRB and SLL designed the study; RAINFOR data network provided the data; AEM analysed the data and wrote the paper. iv Chapter 6 In preparation. AEM, OLP, KGD, TRB and SLL designed the study; RAINFOR data network provided the data; AEM analysed the data and wrote the paper. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. Assertion of moral rights: The right of Adriane Esquivel Muelbert to be identified as Author of this work has been asserted by her in accordance with the Copyright, Designs and Patents Act 1988. © 2016 The University of Leeds and Adriane Esquivel Muelbert v Acknowledgments Bringing a four-year project together in one document showed me how much I have achieved during this process. Looking at all these pages I see a dream becoming reality, which was only possible because of the amazing people that supported me along this journey. I feel particularly lucky. I had Oliver Phillips as my main supervisor who guided me through this intellectual Amazonian adventure and from whom I have learned so much about science and tropical forests. His dedication and patience helped me improve at each of the uncountable supervision meetings. Together with Oliver, I had a stellar team of ecologists as co-supervisors: Kyle Dexter, Tim Baker and Simon Lewis, who were always supportive and inspirational. Working with them was a privilege and I thank them for their help, great ideas and dedication. I further thank Hans ter Steege for contributing with data and ideas for Chapter 3. I was part of the Ecology and Global Change (EGC) research group at the University of Leeds, which helped to expand my understanding of climate change. From EGC I specially thank David Galbraith, who helped to developed Chapter 4, and Sarah Batterman for providing me with a writing retreat and Olivia’s company. EGC gave me amazing friends: Jess Baker, Freddie Draper, Greta Dargie, Sophie Fauset, Martin Gilpin, Michelle Johnson, Joey Talbot, Euridice Honorio, Rosie Goodman, Yunxia Wang and Michelle Kalamandeen. My PhD was part of the T- FORCES project and I had the great help of Gabriela Lopez Gonzalez and Georgia Pickavance, whose organization and patience solve any data issue. Martin Sullivan, Lan Qie (Lainie) and Wannes Hubau were also really helpful in sharing codes and discussing plot issues. I had the chance to dive into the forest for a few months during the course of my PhD. In Nova Xavantina I joined Beatriz Marimon, Ben Hur Marimon Junior and their lovely students who adopted me in 2013 and taught me how to achieve excellence in data collection. Across BR-319 I joined Thaiane de Souza and a dream in an Amazon boot camp that changed my perception of fieldwork. Flavia Costa and her lab hosted me in INPA providing a great and insightful time in Manaus. vi Leeds became a few degrees warmer during my PhD, not only as a consequence of global warming, but driven by the arrival of the Brazilian crew. They brought high quality volleyball, pão de queijo and tight hugs. Julia Tavares, Fernanda Coelho (my great tree id teacher across BR-319), Marta Giannichi, Bruno Cintra, Francisco Diniz, Karina Melgaço, Alfredo Filho, Matheus Grandi and William Goulart. Obrigada pelo carinho, atencão e risadas. Thanks to the Department of Geography things went smooth. The helpful and friendly staff was essential, especially Jacqui Manton, Dom Emery, Emma Sanderson and Fikir Assefa. Here I made amazing friends and learnt from their interesting research topics: Kathryn, Dylan, Liz, Will, Tom(s), Magaly, Heru, Marrie, Marina, Khalil, Rachel, Federico and Ersilia. Among the human geographers I met a special friend from Taipei, Hui-Fang Liu, my yoga guru whom words of wisdom brought things to perspective. I also met Ana Julia Cabrera Pacheco from Yucatan who went through this adventure with me from day one to submission and who I thank for being practicamente familia, for showing me that sí se puede! even when we were under pressure, and for every evening she convinced me to take a break and go for a pint. My friends and family from Brazil join me in this project caring, supporting and making me feel close to our southern island. I thank my siblings Juan and Luíse, Mum and Dad for all the love and understanding, for making any challenge seem easy and for being great friends at all times. I thank Mathew Richardson, who by accident ended up learning quite a lot about how global change affects tropical forests. I thank you for your enthusiasm about my endless results and conclusions, for reading drafts several times and for keeping me smiling all the way through. This thesis is not an individual's work, but one of the fruits from large tree of researchers passionate about the Amazon. It was only possible to analyse data from more than 500 plots monitored at times over 30 years because of those who collected, organized and managed the data from these plots so that humanity could understand and protect the most diverse and fascinating forest on the planet. I dedicate my thesis to every person that contributed to this process from tape measurements and botanical vouches to numbers and names in huge tables of data. I am extremely grateful to have the opportunity to contribute to this team. vii Abstract Intact Amazonian forests are often considered to be in a steady-state, where gains in growth and recruitment are offset by losses in mortality and where net carbon accumulation is close to zero. However, permanent plot data have shown that this ecosystem removes ca. 0.4 Pg of carbon per year from the atmosphere, approximately 5% of annual anthropogenic emissions. This thesis tests several competing hypothesized drivers of detected shifts in the structure and dynamics of intact forest, by assessing changes in functional and floristic composition over the last 30 years in over 100 long-term tree monitoring plots distributed across the Amazon. I first show that the majority of species are restricted to wetter conditions, indicating that stronger and more frequent droughts could threaten many species (Chapter 3). I generated an index of water-deficit affiliation for more than 500 genera and 1800 species (Chapter 3), and demonstrated that this index can predict drought-induced mortality in several drought experiments (Chapter 4). Finally, I document how floristic and functional composition of Amazonian forests has shifted over the last 30 years: forests are increasingly dominated by large-statured taxa, and further, large trees are becoming even larger in absolute size (Chapters 5 and 6). However, relative gains in basal area were similar across size classes and canopy status. In addition, recruits are increasingly comprised of dry-affiliated genera, while the mortality of wet-affiliated genera has increased in plots where the dry season has become more intense. Communities are becoming more dry- affiliated, although these changes still lag behind the drying trend. Overall, this thesis shows the potential vulnerability of Amazonian biodiversity to an increase in aridity and supports the hypotheses that a changing climate and increased atmospheric CO2 are driving changes in Amazonian floristic and functional dynamics.
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