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Ydraulic Architecture of Mangroves

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Ydraulic Architecture of Mangroves Growing on the edge ydraulic architecture of mangroves HEcological plasticity and functional significance of water conducting tissue in Rhizophora mucronata and Nele Schmitz Growing on the edge Print: DCL Print & Sign, Zelzate © 2008 Nele Schmitz © 2008 Uitgeverij VUBPRESS Brussels University Press VUB PRESS is an imprint of ASP nv (Academic and Scientific Publishers nv) Ravensteingalerij 28 B-1000 Brussels Tel. ++32 (0)2 289 26 50 Fax ++32 (0)2 289 26 59 E-mail: [email protected] www.vubpress.be ISBN 978 90 5487 489 8 NUR 922 Legal deposit D/2008/11.161/03 3 All rights reserved. No parts of this book may be reproduced or transmitted in any form or by any means, elec­ tronic, mechanical, photocopying, recording, or otherwise, without the prior written permission of the author and the publisher. Growing on the edge Hydraulic architecture of mangroves: ecological plasticity and functional significance of water conducting tissue in Rhizophora mucronata and Avicennia marina Thesis Submitted in fulfillment of the requirements for the degree of Doctor of Philosophy in Sciences of the Vrije Universiteit Brussel by Nele Schmitz May 2008 Promotors Nico Koedam Laboratory of Plant Biology and Nature Management Vrije Universiteit Brussel Hans Beeckman Laboratory of Wood Biology and Xylarium Royal Museum for Central Africa This research project was a collaboration between the Laboratory of Plant Biology and Nature Management of the Vrije Universiteit Brussel and the Laboratory of Wood Biology and Xylarium of the Royal Museum for Central Africa, Tervuren and was funded by the Institute for the Promotion of Innovation through Science and Technology in Flanders. Research stays abroad were sponsored by the European Commission's Research Infrastructure Action via the Synthesys Project and by the European Cooperation in the field of Scientific and Technical Research programme (COST) on Cell wall macromolecules and reaction wood (CEMARE) via a Short Term Scientific Mission. Fieldwork expeditions were financially supported by the National Fund for Scientific Research (FWO, Belgium), the Schure-Beijerinck-Popping Fonds (Koninklijke Nederlandse Akademie van Wetenschappen, The Netherlands) and the Flemish Interuniversity Council (VLIR). Photos: Nele Schmitz, Elisabeth Robert. KONINKLIJK MUSEUM IWI VOORMIDDEN-AFRIKA Instituut voor de Aanmoediging van Innovatie Vrije MUSÉE ROYAL door W etenschap en Technologie in Vlaanderen TERVUREN DE L'AFRIQUE CENTRALE Universiteit Brussel A Koninklijke rjiznsb milii Nederlandse VLIR s ninii Akademie van U O S Univmity Dcvrlopmtni Cooptrotroo *. SYNTHESYS isnsssns Wetenschappen * SynlliBSJS of systematic resources A ll men by nature desire to know. A r is t o t e l e s A man should live if only to satisfy his curiosity. A Y i d d is h p r o v e r b . Contents Outline o f the thesis 9 General introduction 11 General objective & hypotheses 22 Part I Hydraulic architecture of mangroves: ecological plasticity & 24 functional significance Summarizing A bstract 2 5 Chapter 1 Influence of a salinity gradient on the vessel characters of the 27 mangrove species Rhizophora mucronata Lam. Chapter 2 Comparative anatomy of intervessel pits in two mangrove species 39 growing along a natural salinity gradient in Gazi Bay, Kenya. Chapter 3 Intervessel pit structure and histochemistry of two mangrove 53 species as revealed by cellular UV microspectrophotometry and electron microscopy: intraspecific variation and functional significance Part II Implications of successive cambia for the hydraulic architecture 64 of Avicennia marina Summarizing A bstract 6 5 Chapter 4 Successive cambia development in Avicennia marina (Forssk.) Vierh. 67 is not climatically driven in the seasonal climate at Gazi Bay, Kenya. Chapter 5 A patchy growth via successive and simultaneous cambia: key to 79 success of the most widespread mangrove species Avicennia marina? General conclusion & perspectives 93 References 101 Samenvatting 123 A cbiow ledgements 127 Curriculum vitae 129 Outline o f the thesis Wonder is the beginning of wisdom. 10 Outline o f the thesis Outline of the thesis Ecological wood anatomy is a challenging field of study. It is a quest for environmental information, which is a complex mix of manifold environmental variables intertwined with the trees genetic blueprint, to unravel how trees adapt their cellular make-up for survival under ambient and site-specific conditions, whether predictable or not. Sprouting ideas from the numerous, patiently and carefully observed and described wood samples give rise to carefully stated anatomy-environment relationships. Always alert for new findings in tree physiology fitting these observations, the researcher may be lead to new insights in the trees’ structure and functioning. Therefore, in a second stage, these hypotheses should be tested experimentally for physiological validation. This awareness of the not yet complete fundaments of ecological wood anatomical hypotheses is essential but certainly not undermining the value of ecological wood anatomy. In contrast to physiological studies, there is neither a restriction on the choice of the studied species nor on the study site, the number of samples analysed, the age or the size of the study objects, allowing profound knowledge on formation characteristics of the trees’ wood via comparison of environmentally different locations, species as well as individual trees. Wood anatomy can be studied in view of the technical applications of wood, tree pathology, ecology, dendrochronology but also hydraulics. In this work, the introductionaddresses the c h a l l e n g e for mangrove trees to transport water in their hydraulically stressful environment and the wood anatomical a p p r o a c h to understand the way mangroves successfully respond to these high environmental demands. The current knowledge about the water transport of trees at risk of bubble formation is presented together with the possible solutions to minimize or to prevent these negative impacts. However, despite their ultimate position to study the regulation of the water transport under stress conditions, insight in the hydraulic structure of mangroves, its ecological plasticity and functional significance remains extremely scanty. The h y p o t h e s e s tested in this study are presented. The first part of the thesis highlights the hydraulic architecture of mangroves in relation to the specific requirements of the regularly flooded and saline environment. The study focuses on two species, Rhizophora mucronata m á Avicennia, growing marina under contrasting conditions but with a certain overlap. The f i r s t c h a p t e r starts with the influence of soil water salinity on vessel characteristics and ends with the question why vessel diameters are nearly constant. The s e c o n d c h a p t e r aims to answer this question by searching for a trend in intervessel pit anatomy. The remarkable variation in intervessel pit membrane thickness and electron density is the subject of the t h i r d c h a p t e r , presenting a study of the topochemistry of the intervessel pits of both mangrove species. The second part of the thesis focuses on the formation of wood by successive cambia and its implications for the hydraulic architecture. While the anatomical development of growth layers via successive cambia has been described for some species, the periodicity of the growth layer formation as a whole has never been addressed before. In the f o u r t h c h a p t e r the annual character of the growth layers of Avicennia marina is investigated while c h a p t e r f i v e proposes a growth mechanism via successive cambia and the potential ecological and functional advantage of this peculiar anatomical structure for life in the mangrove environment. The thesis is completed with a general conclusion on the plasticity of the water transport system of mangrove trees, the functional advantage of having successive cambia and this all in view of their survival in an environment characterized by exceptional growth conditions, which are also to some extent unpredictable. 11 General Introduction All things are difficult before they are easy. 12 General Introduction eneral GIntroduction Structure The problem: water transport in mangroves, a risky business 12 ■ The mangrove environment ■ Water transport and its limitations Approach: the added value of ecological wood anatomy in clarifying tree16 functioning ■ The tissue level ■ The cellular level ■ The sub-cellular level General objective & hypotheses 22 ■ Hypothesis I: ecological plasticity within species ■ Hypothesis II: ecological significance of successive cambia 13 General Introduction From the origin of life on land, water uptake and transport against gravitational forces and under the restrictions imposed by the environment are one of the major challenges for plants (Kramer and Boyer, 1995; Kozlowski and Pallardy, 1997; Maseda and Fernández, 2006). Both for growth and species distribution water availability clearly is one of the most determining factors for land plants (e.g. Ball, 1998; Brodribb and Hill, 1999; Pockman and Sperry, 2000; Maherali et‘al., 2004). This is especially true for tail growing trees since tree height is constrained by water-controlled physiological factors (Woodward, 2004; Zaehle, 2005; Holbrook and Zwieniecki, 2008). Nevertheless, a successful forest ecosystem with trees reaching heights of several tens of meters developed along the coasts of the tropical and subtropical climate zone: mangroves (Tomlinson, 1994; Spalding et al., 1997;
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