Ecophysiology of Tropical Tree Crops-Nova Science Pub Inc (2010)

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<p>AGRICULTURE ISSUES AND POLICIES SERIES</p><p>ECOPHYSIOLOGY OF TROPICAL</p><p>TREE CROPS</p><p>No part of this digital document may be reproduced, stored in a retrieval system or transmitted in any form or</p><p>by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no</p><p>expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No</p><p>liability is assumed for incidental or consequential damages in connection with or arising out of information</p><p>contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in</p><p>rendering legal, medical or any other professional services.</p><p>AGRICULTURE ISSUES AND POLICIES SERIES</p><p>Agriculture Issues & Policies, Volume I</p><p>Alexander Berk (Editor)</p><p>2001. ISBN 1-56072-947-3</p><p>Agricultural Conservation</p><p>Anthony G. Hargis (Editor)</p><p>2009. 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ISBN: 978-1-60741-130-7</p><p>Ecophysiology of Tropical Tree Crops</p><p>Fabio DáMatta (Editor)</p><p>2010. ISBN 978-1-60876-392-4</p><p>AGRICULTURE ISSUES AND POLICIES SERIES</p><p>ECOPHYSIOLOGY OF TROPICAL</p><p>TREE CROPS</p><p>FÁBIO DAMATTA</p><p>EDITOR</p><p>Nova Science Publishers, Inc.</p><p>New York</p><p>Copyright © 2010 by Nova Science Publishers, Inc.</p><p>All rights reserved. No part of this book may be reproduced, stored in a retrieval system or</p><p>transmitted in any form or by any means: electronic, electrostatic, magnetic, tape, mechanical</p><p>photocopying, recording or otherwise without the written permission of the Publisher.</p><p>For permission to use material from this book please contact us:</p><p>Telephone 631-231-7269; Fax 631-231-8175</p><p>Web Site: http://www.novapublishers.com</p><p>NOTICE TO THE READER</p><p>The Publisher has taken reasonable care in the preparation of this book, but makes no expressed or</p><p>implied warranty of any kind and assumes no responsibility for any errors or omissions. No</p><p>liability is assumed for incidental or consequential damages in connection with or arising out of</p><p>information contained in this book. The Publisher shall not be liable for any special,</p><p>consequential, or exemplary damages resulting, in whole or in part, from the readers’ use of, or</p><p>reliance upon, this material. Any parts of this book based on government reports are so indicated</p><p>and copyright is claimed for those parts to the extent applicable to compilations of such works.</p><p>Independent verification should be sought for any data, advice or recommendations contained in</p><p>this book. In addition, no responsibility is assumed by the publisher for any injury and/or damage</p><p>to persons or property arising from any methods, products, instructions, ideas or otherwise</p><p>contained in this publication.</p><p>This publication is designed to provide accurate and authoritative information with regard to the</p><p>subject matter covered herein. It is sold with the clear understanding that the Publisher is not</p><p>engaged in rendering legal or any other professional services. If legal or any other expert</p><p>assistance is required, the services of a competent person should be sought. FROM A</p><p>DECLARATION OF PARTICIPANTS JOINTLY ADOPTED BY A COMMITTEE OF THE</p><p>AMERICAN BAR ASSOCIATION AND A COMMITTEE OF PUBLISHERS.</p><p>LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA</p><p>Ecophysiology of tropical tree crops / editor: Fábio DaMatta.</p><p>p. cm.</p><p>Includes bibliographical references and index.</p><p>ISBN 978-1-61324-530-9 (eBook)</p><p>1. Tropical crops--Ecophysiology. 2. Tree crops--Ecophysiology. 3. Plant ecophysiology. I. DaMatta,</p><p>Fábio.</p><p>QK936.E26 2010</p><p>634--dc22</p><p>2009035587</p><p>Published by Nova Science Publishers, Inc. New York</p><p>CONTENTS</p><p>Preface ix</p><p>Abbreviations xi</p><p>Chapter 1 Introduction 1</p><p>Fábio M. DaMatta</p><p>Chapter 2 Bananas: Environment and Crop Physiology 7</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>Chapter 3 Cacao: Ecophysiology of Growth and Production 37</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>Chapter 4 Cassava: Physiological Mechanisms and Plant Traits Underlying</p><p>Tolerance to Prolonged Drought and Their Application for Breeding</p><p>Improved Cultivars in the Seasonally Dry and Semiarid Tropics 71</p><p>Mabrouk A. El-Sharkawy</p><p>Chapter 5 Citrus: An Overview of Fruiting Physiology 111</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores,</p><p>Miguel A. Naranjo, Gabino Ríos, Esther Carrera,</p><p>Omar Ruiz-Rivero, Ignacio Lliso, Raphael Morillon,</p><p>Francisco R. Tadeo and Manuel Talon</p><p>Chapter 6 Coconut Palm: Ecophysiology under Water Deficit Conditions 151</p><p>Fábio P. Gomes and Carlos H. B. A. Prado</p><p>Chapter 7 Coffee: Environment and Crop Physiology 181</p><p>Fábio M. DaMatta, Cláudio P. Ronchi, Moacyr Maestri and</p><p>Raimundo S. Barros</p><p>Chapter 8 Mango: Reproductive Physiology 217</p><p>Thomas L. Davenport</p><p>Chapter 9 Mango: Effects of Preharvest Factors on Fruit Growth, Quality and</p><p>Postharvest Behavior 235</p><p>Mathieu Léchaudel and Jacques Joas</p><p>Contents viii</p><p>Chapter 10 Oil Palm: Ecophysiology of Growth and Production 253</p><p>Ian E. Henson</p><p>Chapter 11 Papaya: Ecophysiology of Growth and Production 287</p><p>Eliemar Campostrini, David M. Glenn and Osvaldo K. Yamanishi</p><p>Chapter 12 Rubber Tree: Ecophysiology and the Land Productivity 309</p><p>V. H. L. Rodrigo</p><p>Chapter 13 Tea: Ecophysiology of Growth and Production 325</p><p>W. A. Janendra M. De Costa, A. Janaki Mohotti</p><p>and Madawala A. Wijeratne</p><p>About the Editor 369</p><p>Contributors 371</p><p>Index 373</p><p>PREFACE</p><p>Plants are frequently exposed to a variety of harsh environmental conditions that</p><p>negatively affect growth and crop yield. An understanding of the responses of crops to their</p><p>environment is thus fundamental to minimizing the deleterious impact of unfavorable climatic</p><p>conditions and to manage crops for maximum productivity. As occurs with most tropical</p><p>plant species, the gaps in our knowledge of the ecophysiology of tropical tree crops are</p><p>incommensurable, though significant advances have occurred in recent years. This book</p><p>highlights both these recent advances and the need for further research on major tropical tree</p><p>crops, considered here in a broader sense, including</p><p>to the shoot.</p><p>Bananas have strong root pressure (Davis, 1961). With this drought tolerance mechanism the</p><p>banana is able to survive long periods of soil water deficit but the disadvantage is that</p><p>production is very sensitive to soil drying. Whether this mechanism applies across the genetic</p><p>diversity of Musa species needs to be established. If genetic variation can be detected then</p><p>there is the possibility of developing cultivars that are less sensitive to soil drying, from the</p><p>point of view of production, but which might not survive long periods of drought. From a</p><p>practical perspective it would be useful to determine the relationship between soil Ψw and gs</p><p>for a range of cultivars in different environments.</p><p>We conclude that the large leaves, high LAI, shallow roots systems or the poor ability of</p><p>banana roots to extract water from the soil cannot account for the sensitivity of the crop to</p><p>soil drying. However, the sensitivity of the root system to drying soil, the ability of the plant</p><p>to send this information to the leaves so that stomata close and once the stomata are closed,</p><p>the capacity of root pressure to maintain the plant in a hydrated state are consistent with the</p><p>widely observed sensitivity of the plant to soil drying supported by anecdotal and</p><p>experimental evidence in the field. Experimental evaluation of this hypothesis is required.</p><p>In addition to pointing to a physiological mechanism that might be modified in the plant</p><p>to produce cultivars more adapted to dry conditions, knowing that the banana plant itself is</p><p>not substantially different from other plants in its use of water leads to questions about the</p><p>technology of applying water to bananas. Lu et al. (2002) pointed out the large difference</p><p>between the amounts of water evaporated by the plant compared with the amount of water</p><p>recommended for irrigation at Darwin, Australia. They suggested that water-use efficiency</p><p>(WUE) at the level of the plantation could be improved by paying attention to the technology</p><p>of irrigation. Robinson (1995, 1996) presents useful discussions of these issues and some</p><p>mathematical aspects are presented by Turner (1995) and recently, and in more detail, by van</p><p>Vosselen et al. (2005).</p><p>Water-Use Efficiency</p><p>With anticipated reductions in water available for cropping in many countries, WUE has</p><p>aroused interest. Water-use efficiency has different definitions depending on the problem</p><p>being investigated and the level of organization of the plant. At the level of the leaf it can be</p><p>expressed as the amount of CO2 fixed per unit of H2O evaporated per kPa of VPD. These data</p><p>can be obtained from instantaneous measurements of leaf gas exchange. They are not</p><p>necessarily correlated with the WUE of the whole plant or the plantation. At the whole plant</p><p>level, WUE may be expressed as the amount of dry matter increase in the plant per unit of</p><p>water evaporated from the plant. At the crop level, the economic yield is important and the</p><p>WUE may be expressed as kilogram of fresh fruit per unit of water used. In this last case it is</p><p>necessary to take account of the water lost from the soil or trash to the atmosphere as well as</p><p>that lost in deep drainage because the water lost from the plant is only a proportion of that lost</p><p>from the system. In this last case, WUE can be increased by increasing the proportion of</p><p>water in the system that flows through the plant.</p><p>Bananas: Environment and Crop Physiology</p><p>19</p><p>Jones (1992) analyzed the components of WUE taking into account the life cycle of the</p><p>plant. The stomatal response of banana would fit within the “optimistic-responsive” category</p><p>indicating that the plant will be quite productive when water supply is adequate, and will</p><p>experience reduced damage during short periods of drought. Evidence for the banana suggests</p><p>that closed stomata caused by soil water deficit mean the plant has switched to a “survival”</p><p>mode, rather than just reduced damage.</p><p>Farmers are interested in plants that have high yields whether they are irrigated or</p><p>rainfed. Plant breeders need a simple method of evaluating large numbers of progeny from</p><p>breeding schemes so that promising genotypes can be rapidly selected. For bananas,</p><p>Bananuka et al. (1999) used leaf water retention capacity to evaluate the tolerance of several</p><p>Musa genotypes to drought. The ability of a leaf to retain water is determined very simply by</p><p>severing the leaf, weighing it, allowing it to dry for 48 h, reweighing and determining dry</p><p>weight of the leaf. Clarke and McCaig (1982) investigated this technique for use in wheat</p><p>breeding schemes in the Americas and concluded that the water loss rate of severed leaves</p><p>was a suitable method for distinguishing between genotypes of wheat that were tolerant of</p><p>drought. Drought tolerance was evaluated by comparing the yield of genotypes in rainfed</p><p>plots with yields from irrigated plots. We examined the published data of Clarke and McCaig</p><p>(1982), expressed drought resistance as the yield from rainfed plots divided by the yield from</p><p>irrigated plots and plotted these data against the rate of drying of excised leaf segments, a</p><p>measure of the leaf water retention capacity. We found no significant correlation (P = 0.13, n</p><p>= 8) between these two parameters. Since leaf water retention was not related to drought</p><p>tolerance in wheat, but had been used by Bananuka et al. (1999) in a range of Musa</p><p>genotypes, we undertook a similar analysis on their data. We assumed firstly that all cultivars</p><p>had a similar leaf number at the beginning of drying, and secondly, that the number of live</p><p>leaves at the end of 32 d of drying reflected the drought resistance of the six banana cultivars</p><p>investigated and plotted this against the published values of leaf water retention capacity.</p><p>There was no significant correlation (P = 0.19, n = 6) between the two parameters for the</p><p>banana genotypes. Both Clarke and McCaig (1982) and Bananuka et al. (1999) found that the</p><p>rate of leaf drying was different between cultivars and based their conclusions on this</p><p>difference. Our analyses would suggest that leaf water retention capacity, as a proxy for</p><p>drought resistance or WUE, should be treated very cautiously. In bananas, there is a need to</p><p>have yield data for irrigated and rainfed plots so that drought tolerance can be quantified in</p><p>these terms.</p><p>An alternative approach to WUE is to evaluate the amount of water available in the</p><p>system and then work out how best to arrange for most of it to flow through the banana plant.</p><p>This would involve management strategies, in addition to new germplasm, and may be a more</p><p>rewarding way forward than simply evaluating germplasm for drought resistance or tolerance</p><p>in a range of environments.</p><p>Tanny et al. (2006) used the energy balance and eddy covariance approach to measure</p><p>water use of bananas, cv. ‘Grand Nain’ (AAA, Cavendish subgroup), growing under</p><p>protected cultivation in Israel in the summer (June). The value of this work in the current</p><p>context is the separate measurement of evaporation from the soil from that of the canopy</p><p>which provides a measure of plant transpiration at the crop level. The plants were drip</p><p>irrigated with 7 or 8 mm d-1 and 28% of the land area was “wet” from the irrigation water</p><p>from the drippers. Mean water use was 5.6 mm d-1 with almost no evaporation from the soil</p><p>(0.1 mm d-1). Net radiation was 14.65 MJ m-2 d-1, enough energy to evaporate 6.0 mm H2O</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>20</p><p>d-1. Since little water was evaporated from the soil, the measured evaporation was taken as</p><p>transpiration. An increase in water application from 7 to 8 mm d-1 during the study did not</p><p>change the evaporation from the crop. The amount of water applied to the plants under</p><p>protected cultivation was about 70% of that applied in the field. In this environment, the use</p><p>of protected cultivation produced considerable savings in irrigation. It would be of</p><p>considerable interest to</p><p>compare water use of bananas grown as an understory crop, especially</p><p>if the root zones of the bananas and overstory did not overlap to a large extent.</p><p>Variation in Stomatal Conductance Between Genotypes</p><p>Ekanayake et al. (1994) investigated the ability of different genotypes of Musa to adapt to</p><p>drought in the field by measuring gs in the morning and afternoon. In this case, the soil water</p><p>content is unlikely to change significantly between measurements but the leaf-to-air vapor</p><p>pressure difference will increase as temperature rises. For the plant, it is a strategy for</p><p>increasing WUE (Jones, 1992). Genotypic differences in this character are evident in a</p><p>number of plant species, with differences apparent between and within species (Jones, 1992).</p><p>Ekanayake et al. (1994) found differences among Musa genotypes. Those genotypes that</p><p>tended to restrict stomatal opening in the afternoon were classed as “water savers” and could</p><p>therefore be expected to tolerate short periods of soil water deficit in contrast to those whose</p><p>stomata remained open in the afternoon. The cvs. ‘Bluggoe’ (ABB) and ‘Fougamou’ (ABB)</p><p>showed the greatest differences in leaf conductance between morning and afternoon while</p><p>cvs. ‘Bobby Tannap’ (ABB) and ‘Valery’ (AAA, Cavendish subgroup) maintained their gs</p><p>throughout the day. They concluded that there was variation in response to drought among the</p><p>genotypes in the ABB genomic group that was worth further investigation.</p><p>Thomas et al. (1998) used controlled conditions to separate the effects of VPD and</p><p>temperature on gs of cvs. ‘Williams’ (AAA, Cavendish subgroup), ‘Lady Finger’ (AAB) and</p><p>‘Bluggoe’ (ABB). Their data clearly show that gs of cv. ‘Williams’ is much more sensitive to</p><p>leaf to air vapor pressure difference than that of cv. ‘Bluggoe’, decreasing as the vapor</p><p>pressure deficit increased. At a vapor pressure difference of 5 kPa, there was no difference in</p><p>gs between either cultivar with differences increasing under more humid conditions. The work</p><p>of Ekanayake et al. (1994) and Thomas et al. (1998) remind us that the stomata of bananas</p><p>respond to the aridity of the air as well as to soil drying and that there is genetic variation in</p><p>this trait.</p><p>ROOT SYSTEM</p><p>Architecture</p><p>The architecture of the root system is its arrangement in the soil and so it has a plant and</p><p>edaphic component. In the bananas, roots arise in groups of 2 to 4 from primordia at the inner</p><p>edge of the cortex of the corm. These main or primary roots give rise to secondary roots that</p><p>support tertiary roots. Each class of root is thinner than the root that supports it, grows more</p><p>slowly (Lecompte et al., 2001) and is much shorter in length. Main or cord roots may be</p><p>Bananas: Environment and Crop Physiology</p><p>21</p><p>several meters long, secondary roots are usually less than 1 m and tertiary roots are several</p><p>centimeters long. The extension of the main roots provides new sites for the development of</p><p>secondary roots that have a much shorter life than that of the main roots. The same pattern</p><p>exists between secondary and tertiary roots. Thus, for banana the main or primary roots</p><p>emerging from the corm provide the framework of the root system that extends well out from</p><p>the plant. The secondary and tertiary roots explore the volume of soil adjacent to the primary</p><p>roots. Studies of the banana root system have therefore focused on the development and</p><p>extent of the primary roots and the factors affecting the growth and development of the</p><p>secondary and tertiary roots.</p><p>Draye (2002a) reviewed the architecture of the banana root system especially in relation</p><p>to genetics. Root architecture has been studied using soil excavation (Araya, 2005),</p><p>simulation (Draye et al., 2005) and manipulative experiments (Lecompte et al., 2001, 2005).</p><p>Soil excavation is laborious but it provides data on the distribution of the root system at a</p><p>point in time and is useful for informing management practices. Over the years numerous</p><p>studies of this type have been undertaken, some more comprehensive than others, depending</p><p>on the objectives of each study. For simulation, conceptual and mathematical relationships</p><p>among the components of the root system need to be established to explore the simulated</p><p>changes in time and space. The advantages of simulation lie in the ability to ask “what if” and</p><p>then change a mathematical relationship or concept and see what happens. Thus many</p><p>“thought experiments” can be done in a short time. The difficulty is relating the precise</p><p>calculations of the simulation to the field where there is considerable variation in space and</p><p>time in the soil in which roots grow. Nonetheless, if simulations are used to complement field</p><p>and laboratory work, then useful progress can be made.</p><p>To reduce the amount of effort needed to undertake excavations of whole root systems,</p><p>Blomme et al. (2005) investigated a number of methods for indirectly measuring the root</p><p>system of 31 genotypes of Musa in southeastern Nigeria. The methods included early</p><p>screening, that sought a relationship between the root system of nursery plants and mature</p><p>plants in the field; allometric relationships between root and shoot characters in field-grown</p><p>plants; soil core sampling; and electrical capacitance. Only the soil core sampling gave useful</p><p>predictive power, with two samples per plant giving 80% accuracy. The soil core sampling</p><p>was 20 times faster than complete excavation of the root system. Draye et al. (2005) used</p><p>their simulation model of the banana root system to evaluate different parameters of soil core</p><p>methods for measuring banana root systems. Of crucial importance are the distance of the</p><p>cores from the plant, the number of cores taken and the size of the cores. Precision in</p><p>estimating the size of the root system is increased by sampling close to the plant (20 cm) and</p><p>having a large number (8) of large cores (25 cm). Draye et al. (2005) point out that their</p><p>calculations are indicative and should not be taken as firm recommendations but it is the</p><p>proximity to the plant that has the greatest impact on accuracy and precision.</p><p>The paper of Araya (2005) provides data on the root distribution of several Musa</p><p>genotypes in Central America. The total excavated fresh weight of roots varied from 0.8 kg</p><p>for cv. ‘Valery’ (AAA, Cavendish subgroup) to more than 3.5 kg for cv. ‘Yangambi km5’</p><p>(AAA), showing the large difference in size of the root system between genotypes. His paper</p><p>also provides data on the changes in the root system during development of the plant and thus</p><p>has a “dynamic” component.</p><p>Lecompte et al. (2001) proposed a method for reconciling the “static” components of root</p><p>growth, measured at the one time, with the ‘dynamic’ components that change over time.</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>22</p><p>They used cv. ‘Grande Naine’ (AAA, Cavendish subgroup) for their studies in rhizotrons</p><p>(using two soil types) and in the field. The distance from the root cap to the appearance of the</p><p>first lateral on any root, termed the length of the unbranched zone, was positively correlated</p><p>with the growth rate of the root up to the time of measurement. For roots with an unbranched</p><p>zone that varied from 4 to 24 cm, the growth rate increased linearly from 0.5 to 3.5 cm d-1, an</p><p>increase of 0.15 cm d-1 in growth rate for each centimeter of unbranched root length. The</p><p>apical diameter indicated the potential for the root to grow, with large roots growing more</p><p>rapidly than smaller roots. However, for any root class (primary, secondary or tertiary) the</p><p>length of the unbranched zone was the indicator of actual growth. Armed with this knowledge</p><p>it is possible to interpret the growth of roots in different situations, whether between cultivars,</p><p>fields, plants or stages of growth.</p><p>Structure</p><p>Lecompte et al. (2005) explored the relationship between the diameter of the root tip and</p><p>the class of root, the variation of root tip diameter within</p><p>classes and the effect of soil</p><p>compaction on this variability. The diameter of the root tip is easy to measure and, as</p><p>Lecompte et al. (2005) point out, across a number of plant species has been related to the size</p><p>of the root meristem, axial growth and its duration, root anatomy, water transport and</p><p>capacity of the root to penetrate media. For the primary roots of cv. ‘Grande Naine’ (AAA,</p><p>Cavendish subgroup) growing in an andosol, the apex ranged from 0.6 to 2.1 mm diameter,</p><p>for secondary roots from 0.09 to 0.52 mm and for tertiary roots from 0.06 to 0.27 mm. The</p><p>mean apical diameters and their coefficients of variation were 1.46 mm (23%) for primary</p><p>roots, 0.21 mm (40%) for secondary roots and 0.12 mm (35%) for tertiary roots. Increasing</p><p>soil compaction from 0.66 to 0.81 g cm-3 had no effect on the variability in root diameter in a</p><p>field experiment but there were some effects in a glasshouse experiment. Across the different</p><p>classes of root there was a relationship between the diameter of the root and the diameter of</p><p>the roots arising from it but the relationship was not linear. Lecompte et al. (2005) brought</p><p>together data for 12 different plant species, including monocots and dicots, annuals and</p><p>perennials and showed that the data for banana fitted within the general picture. Roots with an</p><p>apical diameter of 0.5 to 2.0 mm produce laterals that have a diameter in the range of 0.1 to</p><p>0.4 mm. Roots with a larger apical diameter of 5 to 13 mm produce laterals with diameters in</p><p>the range of 0.45 to 0.90 mm.</p><p>The lateral roots are the main interface between the plant and the soil and so it is</p><p>important to know about their structure and function. Lateral roots arise from primordia at the</p><p>pericycle. The primordia are laid down acropetally at the root apex and in a series of files,</p><p>lines or poles that are based in the proto-xylem and run along the axis of the root. To account</p><p>for the variable distances between lateral roots one possibility is that there is variation in the</p><p>initiation of root primordia. Another view is that the primordia are laid down regularly, but it</p><p>is whether or not they develop into a lateral root that explains the variability. Draye (2002b)</p><p>investigated the effects of root growth and vascular structure on the initiation and</p><p>development of lateral roots. Using the banana genotypes ‘Agbagba’ (AAB), ‘Grande Naine’</p><p>(AAA, Cavendish subgroup) and ‘Pisang Lilin’ (AA) he found that the distance between files</p><p>(vascular structure) of lateral root primordia around the circumference of the pericycle was</p><p>very stable across classes of root and genotypes. The average distance between files was 63</p><p>Bananas: Environment and Crop Physiology</p><p>23</p><p>μm in roots grown in water and slightly further apart at 76 μm in roots grown in sand. Thus</p><p>roots of greater diameter had more files of lateral root initials around their larger steles.</p><p>Within a file there was a strong positive relationship between the diameter of the root apex</p><p>and the distance between laterals in that file (root growth factor). In a file the distance</p><p>between laterals ranged from 1 to 4 mm and this was almost directly proportional to the apical</p><p>diameter of the root, with some differences between genotypes. Because there are a large</p><p>number of files in each root the distance between laterals on the root irrespective of the file</p><p>ranged from 0.05 to 0.14 mm and was independent of the size of the root apex. Draye (2002b)</p><p>proposed a model framework to differentiate the effects of root growth (lateral root initiation</p><p>and cell number and size influencing the distance between laterals in each file) and vascular</p><p>structure (stellar diameter and distance between files on the pericycle) on the distance</p><p>between laterals on a root. This analysis suggested that root growth would be the major, but</p><p>not only, influence on the density of branching in roots.</p><p>Roots depend on the shoots for their carbon supply for growth and so manipulation of the</p><p>carbon supply changes root growth and architecture. Under conditions of reduced carbon</p><p>supply the allocation of carbon within the root would be between the growth of the main</p><p>apex, where primordia for new laterals would be laid down, and the growth of lateral roots.</p><p>Since carbon flows along the primary root before reaching the first and then the second order</p><p>laterals, one may expect those roots closest to the source would benefit most. Lecompte and</p><p>Pagès (2007) grew banana cv. ‘Grand Naine’ (AAA, Cavendish subgroup) under high (field,</p><p>29 mol photons m-2 d-1) and low (shaded greenhouse, 6 mol photons m-2 d-1) light regimes and</p><p>studied the effect on root growth and architecture. Shading reduced the number of primary</p><p>roots arising from the corm by 12% but had no effect on the elongation rates of those roots.</p><p>Shading reduced branch density of the first order lateral roots by 32%, their diameter by 14%</p><p>but increased their growth rate by 16%. The effect of shading was much greater on the second</p><p>order laterals whose diameter was reduced by 31%, growth rate by 23% and branching by</p><p>11%. So, while the general principle of those organs closest to the source being best served,</p><p>was evident, the allocation of carbon among the different functions within the root orders</p><p>differed qualitatively and quantitatively. Since the second order laterals are the most affected,</p><p>and these have the greatest interface with the soil, then the impact of changes in their</p><p>structure and function can be expected to have considerable impact on the capacity of the</p><p>plants to absorb water and nutrients.</p><p>Bananas and plantains grow in areas where solar radiation varies seasonally and spatially.</p><p>Solar radiation on an overcast day is about 20% of that on a clear day. Extended cloudiness</p><p>could affect the amount of carbon fixed by the canopy and this may have consequences for</p><p>root growth and function. It is possible in extended periods of cloudy weather that the root</p><p>system would be affected and the roots that survive would face different challenges when the</p><p>cloudy weather ended.</p><p>Function</p><p>Plant roots have a number of functions including the uptake of nutrients and water. Lahav</p><p>(1995) summarized the work on banana nutrition, mainly from the perspective of nutrient use</p><p>in a plantation. Johns and Vimpany (1999a), using cv. ‘Williams’ (AAA, Cavendish</p><p>subgroup), investigated the effect of lime and high potassium (K) application on soil and</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>24</p><p>plant chemistry and plant growth, including roots. With their data they were able to construct</p><p>models of the relationship between chemical composition and plant performance. They show</p><p>the empirical nature of such relationships and the need to take considerable care in extending</p><p>them to locations different from the one in which they were established. Delvaux et al. (2005)</p><p>reviewed ion absorption by banana roots, including for a range of triploid genotypes. For</p><p>banana, K and nitrogen are the elements absorbed in greatest amounts. Bananas require a</p><p>large amount of K compared with other species because the plant holds a high amount of</p><p>water per unit area of land. For example, a standing crop of bananas at anthesis will contain</p><p>the equivalent of 30 mm of water, whereas a forest may contain 15 mm and a crop of wheat at</p><p>anthesis about 3 mm. If the molar concentration of K in the plant tissues is the same in all</p><p>three situations then to establish, bananas need to absorb 10 fold more K than wheat, for</p><p>example. In ratoon situations a proportion of K is recycled to the next crop either by</p><p>redistribution within the plant or through the return of organic matter from the plant to the</p><p>soil. Roots require energy to absorb K from the soil and protons are excreted from roots into</p><p>the rhizosphere to maintain the cation/anion balance of the root (Delvaux et al., 2005). The</p><p>excreted protons may react with clay minerals, changing the chemistry of the rhizosphere</p><p>increasing the availability</p><p>of elements such as calcium and magnesium that are beneficial to</p><p>the plant or of aluminum that may become toxic. In addition, bananas roots are able to absorb</p><p>NH4</p><p>+ in preference to NO3</p><p>– and this further contributes to the net excretion of protons.</p><p>Delvaux et al. (2005) point out the importance of the rhizosphere for the plant and the need</p><p>for greater knowledge of its role. It is important not only for water and nutrient uptake but for</p><p>interaction of the plant with soil biota, organic constituents, gases and minerals.</p><p>Recently there has been interest in the silicon (Si) uptake of bananas because of its</p><p>perceived benefits summarized by Henriet et al. (2006) who addressed several questions.</p><p>Does an increased supply of Si improve plant growth in banana under optimal conditions?</p><p>What is the mechanism of Si uptake? Is the transpiration stream the dominant factor</p><p>controlling uptake of Si and its distribution within the plant? Is there genetic variation in the</p><p>response of bananas to increased supply of Si? Henriet et al. (2006) examined the response of</p><p>cv. ‘Grande Naine’ (AAA, Cavendish subgroup) and selections of M. acuminata subsp.</p><p>banksii (AA) and M. balbisiana (BB, Tani) to Si supply under controlled conditions. Silicon,</p><p>at concentrations normally found in soil solutions, did not influence the growth of any of</p><p>three genotypes. The amount of Si absorbed by the plant was a function of the concentration</p><p>of Si in the nutrient solution and the amount of water transpired by the plants. However, this</p><p>relationship was influenced by the Si concentration in the solution. At lower concentrations</p><p>(0.02 to 0.83 mM Si) there was evidence that more Si was absorbed than might be expected</p><p>by the water uptake and so at these concentrations an energy-dependent mechanism may be</p><p>involved. There was no evidence that genotype affected Si uptake, but there were differences</p><p>in the way Si was distributed within the plants, especially at lower concentrations of Si. In</p><p>this case the M. acuminata subsp. banksii plants sequestered more Si in the tissues closer to</p><p>the source than did the M. balbisiana genotype.</p><p>The supply of oxygen to banana root systems in the field has long been a concern</p><p>(Popenoe, 1941) and is dealt with in agronomic practice by extensive drainage systems when</p><p>growing bananas for export (Stover and Simmonds, 1987). Turner (2005) summarized recent</p><p>research on the effects of oxygen deficiency on the nutrient uptake and hydraulic conductivity</p><p>of banana roots. This work (Aguilar et al., 2003) showed that the gradient in oxygen</p><p>concentration from the bathing solution to the stele was quite high and that only a small</p><p>Bananas: Environment and Crop Physiology</p><p>25</p><p>decrease in oxygen concentration (3 kPa) external to the root would induce anoxia in the stele</p><p>and reduce nutrient transfer to the stele. This work has been done on primary roots arising</p><p>directly from the corm. What happens in lateral roots has yet to be determined. It is likely that</p><p>the principles established by Aguilar et al. (2003) for primary roots will apply but the lateral</p><p>roots are thinner and their connection to the shoot is more remote and more tortuous. The</p><p>significance of aerenchyma in primary roots (Aguilar et al., 1999) for supplying oxygen to</p><p>lateral roots needs to be evaluated.</p><p>Oxygen deficiency quickly kills the root apex because even in aerated soils its high</p><p>respiration rate contributes to the low oxygen concentrations found within it. Death of the</p><p>root tip causes several lateral roots to arise not far behind the dead apex and in the field this</p><p>symptom is referred to as “chicken feet” or “witches broom”. This symptom was thought to</p><p>be caused by dry soils and high concentrations of nutrients, especially K, in soils in New</p><p>South Wales, Australia (Johns and Vimpany, 1999b). Experiments that included a range of</p><p>soil water deficits and K applications in excess of that normally applied to bananas, failed to</p><p>link the “witches broom” symptoms with these factors. Any increase in root death caused by</p><p>these factors tended to affect the whole root system rather than just the root tip (Johns and</p><p>Vimpany, 1999b).</p><p>REPRODUCTIVE SYSTEM</p><p>Bunch Initiation</p><p>In banana, the inflorescence (bunch) is initiated at the apex of the vegetative plant and</p><p>subsequently the nodes of flowers that become the hands of fruit begin to differentiate. The</p><p>first three to 18 nodes of the inflorescence form female flowers that become the fruit of</p><p>commerce. At the time of bunch initiation about 11 leaves are present within the pseudostem</p><p>(Summerville, 1944). After these leaves emerge the bunch appears at the top of the</p><p>pseudostem at anthesis. Day-neutral plants do not depend on photoperiod for floral induction</p><p>(Lincoln et al., 1982) and banana falls into this category. Bunch initiation would be</p><p>“autonomous” according to the terminology used by Wilkie et al. (2008). Bunches emerge</p><p>(anthesis) at any time of the year where the plant is grown, although the number of bunches</p><p>emerging may be influenced seasonally by environmental and edaphic factors. If photoperiod</p><p>does not influence bunch initiation then the development of the plant can be described by</p><p>growing-degree-days (GDD, with units of ˚C days). This can be demonstrated in planting date</p><p>experiments where, for each planting date the GDD from planting to bunch emergence is</p><p>expected to be the same, other things being equal. However, Turner and Hunt (1987) pointed</p><p>out that for banana cv. ‘Williams’ (AAA, Cavendish subgroup) growing in the subtropics, the</p><p>GDD was not the same for three different planting dates suggesting some other factor,</p><p>perhaps photoperiod, was involved in bunch initiation.</p><p>Lassoudière (1978a, 1978b) conducted planting date experiments with banana cv. ‘Poyo’</p><p>(AAA, Cavendish subgroup) over 5 yr in Ivory Coast (5˚30’N). In 1971/1972 suckers were</p><p>planted in a ferralitic soil on four occasions at Azaguié. At Nieky, corm pieces with buds</p><p>were planted on six occasions in 1973/1974 in a virgin organic soil and on five occasions in</p><p>1974/1975 in an organic soil that had been subjected to agriculture for some time. Using these</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>26</p><p>data from Ivory Coast we calculated the GDD from planting until bunch emergence of the</p><p>plant crop for each planting date (Figure 3). There was variation in the GDD for the different</p><p>locations, soils and planting material, which may be expected. More importantly there was</p><p>variation in the GDD between planting dates within locations where the crops planted earliest</p><p>in the year had the least GDD. From these data we can say that it is likely that a factor other</p><p>than temperature is influencing bunch initiation in bananas, a similar conclusion reached by</p><p>Turner and Hunt (1987) for cv. ‘Williams’ in a sub-tropical environment.</p><p>Planting date, day number of the year</p><p>0 50 100 150 200 250 300 350</p><p>G</p><p>D</p><p>D</p><p>fr</p><p>om</p><p>p</p><p>la</p><p>nt</p><p>in</p><p>g</p><p>to</p><p>b</p><p>un</p><p>ch</p><p>e</p><p>m</p><p>er</p><p>ge</p><p>nc</p><p>e,</p><p>C</p><p>o da</p><p>ys</p><p>0</p><p>1000</p><p>2000</p><p>3000</p><p>4000</p><p>Azaguie, Ferralitic soil</p><p>Nieky, Virgin organic soil</p><p>Nieky, Old organic soil</p><p>Figure 3. The effect of planting banana cv. ‘Poyo’ (AAA, Cavendish subgroup) at different times of the</p><p>year at three sites in Ivory Coast (Lat 5°N) on the growing degree days (GDD) from planting until</p><p>bunch emergence of the plant crop. Data were compiled from Lassoudière (1978a, 1978b). Redrawn</p><p>from Turner et al. (2007) with permission of Brazilian Society of Plant Physiology.</p><p>Herndl et al. (2008) proposed a method for identifying factors that contribute to early or</p><p>late flowering in cereals. In this method the GDD of the early planting date is plotted on the x</p><p>axis against the GDD of the later planting dates, for a range of cultivars. The 1:1 line</p><p>indicates no effect of photoperiod or temperature (independent of GDD) on plant</p><p>development, and is the “earliness per se” line (Figure 4). Points falling above or below the</p><p>1:1 line indicate an effect of temperature</p><p>on earliness per se. Points below the 1:1 line</p><p>indicate sensitivity to photoperiod where the GDD of later planted crops is less than that of</p><p>earlier planted crops. The larger the difference between the GDD sums of the early and later</p><p>planted crops the greater the sensitivity to photoperiod. We used this method of analysis for</p><p>crops of bananas planted at different times in Ivory Coast, a tropical location (Lat 5˚N)</p><p>(Lassoudière 1978a, 1978b), and in New South Wales, Australia, a sub-tropical location (Lat</p><p>29˚S) (Turner and Hunt 1987) (Figure 4).</p><p>The crops grown in Ivory Coast matured more rapidly (fewer GDD) than those in</p><p>Australia as they had lower values of GDD for all planting dates (Figure 4). Within a planting</p><p>series (Azaguie, Nieky, Alstonville), the later planting dates took longer to mature because</p><p>Bananas: Environment and Crop Physiology</p><p>27</p><p>they had more GDD from planting until bunch emergence, and these points are located above</p><p>the 1:1 line (Figure 4). In these crops, this implies an effect of temperature that is independent</p><p>of GDD, on earliness per se. For Alstonville, with its subtropical environment, the cooler</p><p>temperatures experienced in the winter may delay plant development more than expected by</p><p>the fewer GDD accumulated at this time of year. However, a similar delay is observed in</p><p>Ivory Coast but the mean daily temperatures experienced there (23-28˚C) are above those at</p><p>Alstonville (13-24˚C). For the data from Turner and Hunt (1987) at Alstonville, we explored</p><p>this further by plotting the cumulative bunch initiation (taken as the appearance of the 11th</p><p>last leaf, (Summerville, 1944)) against GDD and superimposing the photoperiod upon these</p><p>graphs. Data were available for three crop cycles (plant, ratoon 1 and 2) at three planting</p><p>dates. Here we present the data for the November planting date (Figure 5) since a similar</p><p>pattern appeared in the data for the January and March planting dates. During the time when</p><p>the photoperiod was less than 12 h, there is a change in the slope of the cumulative curves</p><p>indicating a slowing of the rate of initiation of bunches in each of the three crop cycles. The</p><p>change of slope is more marked in the ratoon crops than in the plant crop. These periods</p><p>correspond to the cooler seasons of the year and may indicate an effect of temperature on the</p><p>“earliness per se” factor in banana cv. ‘Williams’. This is consistent with the data in Figure 4</p><p>suggesting that temperature, other than GDD, influences “earliness per se” in banana.</p><p>However, it is not clear what factor(s) might have the same effect in the tropics of Ivory</p><p>Coast.</p><p>GDD from planting to bunch emergence in earliest crop, Codays</p><p>0 1000 2000 3000 4000 5000</p><p>G</p><p>D</p><p>D</p><p>in</p><p>la</p><p>te</p><p>r f</p><p>lo</p><p>w</p><p>er</p><p>in</p><p>g</p><p>cr</p><p>op</p><p>s,</p><p>C</p><p>o da</p><p>ys</p><p>0</p><p>1000</p><p>2000</p><p>3000</p><p>4000</p><p>5000</p><p>Azaguie</p><p>Nieky virgin organic soil</p><p>Nieky old organic soil</p><p>Alstonville</p><p>1:1 line</p><p>Figure 4. The relationship between the growing degree days (GDD) from planting until bunch</p><p>emergence in the plant crop in planting date experiments in Ivory Coast (Azaguie, Nieky, 5°N) and</p><p>Australia (Alstonville, 29°S). The 1:1 line represents earliness per se. Data for Ivory Coast (Azaguie</p><p>and Nieky) and for Australia (Alstonville) were compiled from Lassoudière (1978a, 1978b) and Turner</p><p>and Hunt (1987), respectively. Redrawn from Turner et al. (2007) with permission of Brazilian Society</p><p>of Plant Physiology.</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>28</p><p>Growing degree days from planting, C0days</p><p>0 2000 4000 6000 8000 10000</p><p>C</p><p>um</p><p>ul</p><p>at</p><p>iv</p><p>e</p><p>bu</p><p>nc</p><p>h</p><p>di</p><p>ffe</p><p>re</p><p>nt</p><p>ia</p><p>tio</p><p>n,</p><p>%</p><p>0</p><p>20</p><p>40</p><p>60</p><p>80</p><p>100</p><p>P</p><p>ho</p><p>to</p><p>pe</p><p>rio</p><p>d,</p><p>d</p><p>ec</p><p>im</p><p>al</p><p>h</p><p>ou</p><p>rs</p><p>10</p><p>11</p><p>12</p><p>13</p><p>14</p><p>15</p><p>Plant Crop</p><p>Ratoon 1 Crop</p><p>Ratoon 2 crop</p><p>Photoperiod</p><p>12 h photoperiod</p><p>Figure 5. The cumulative bunch differentiation of three crop cycles of cv. ‘Williams’ banana (AAA,</p><p>‘Cavendish’ subgroup) planted at Alstonville, NSW (Lat 29°S). The bunch is assumed to differentiate</p><p>11 leaves before it appears at the top of the pseudostem. Curves are plotted against cumulative growing</p><p>degree days from planting on 16 November 1977. The oscillating line is photoperiod (decimal hours)</p><p>and the horizontal line defines the 12 h photoperiod. Data were compiled from Turner and Hunt (1987).</p><p>Redrawn from Turner et al. (2007) with permission of Brazilian Society of Plant Physiology.</p><p>In Honduras (15˚N) Dens et al. (2008) found that removal of the bunch and leaves on the</p><p>parent hastened the development of the ratoon crop in long days but the same treatment had</p><p>no effect on development when conducted during short days. They concluded that an</p><p>environmental factor was contributing to floral induction in banana because the effect of the</p><p>treatment in hastening development of the ratoon was overridden in the season with shorter</p><p>days. While banana is currently regarded as day-neutral for floral induction because it does</p><p>not depend on photoperiod for flowering, there is evidence that environmental factors delay</p><p>floral development, independent of GDD. If this factor was short photoperiod, then bananas</p><p>may be classified as quantitative long day plants.</p><p>Flower Development</p><p>The inflorescence is a terminal spike comprising of a series of nodes of flower clusters</p><p>(hands) that are subtended by bracts. The female flowers occupy the basal nodes and the male</p><p>flowers the apical nodes. The female ovary is inferior with three locules that each contains an</p><p>axile placenta. The ovules are in two or four rows in each locule. The megasporogenesis and</p><p>megagametogenesis of Musa spp. are typical of angiosperms. The ovule is anatropous,</p><p>bitegmic and crassinuclear. Both integuments form the micropyle. The megaspore is</p><p>monosporic and gametogenesis is polygonal. The nucellus is massive. The megasporocyte</p><p>undergoes the usual meiotic division to form a linear tetrad of four cells. The embryology is</p><p>Bananas: Environment and Crop Physiology</p><p>29</p><p>of the Asterad type (White, 1928; Bouharmont, 1963; Dahlgren et al., 1985; Goldberg, 1989;</p><p>Johri et al., 1992).</p><p>Floral initiation begins when the indeterminate vegetative apex is transformed into a</p><p>determinate reproductive apex; the shoot apex ceases to produce leaves and starts to produce</p><p>floral parts. The inflorescence bears three to 15 or more clusters of female flowers and 150 to</p><p>300 clusters of male flowers. Summerville (1944) proposed that the upper limit of</p><p>inflorescence size was set by the size of the meristem at the time of transformation, thus at</p><p>floral initiation environmental conditions that affect general vegetative development will</p><p>affect fruit production. This notion has yet to be tested experimentally although within a</p><p>cultivar, large plants produce large bunches of fruit. Within the inflorescence the</p><p>transformation from female to male flowers is marked by a sudden decline in ovary length</p><p>that is first noticeable when the inflorescence is midway up the pseudostem and the female</p><p>ovaries have reached approximately 10 mm in length.</p><p>The sequence of floral initiation, formation of the ovule primordium and the megaspore</p><p>mother cell occurs while the inflorescence is inside the pseudostem. Consequently, when the</p><p>inflorescence emerges they are almost at anthesis. When the inflorescence is midway up the</p><p>pseudostem the megasporangium (ovule) is differentiating, it appears as a rounded</p><p>protuberance growing at right angles from the placental wall. It is at first atropus and by</p><p>differential growth becomes anatropous with its micropyle pointing towards the placental</p><p>wall. The inner integuments have already formed when the archesporium arises from any sub-</p><p>epidermal cell near the summit of the nucellus. It is easily distinguished from the surrounding</p><p>cells by its relatively large size and becomes the megaspore mother cell. The differentiation</p><p>of the archesporium takes place before the differentiation of the outer integument and when</p><p>the megasporangium is half anatropous. The ovules</p><p>have almost attained maximum size when</p><p>the megaspore mother cell begins to divide. When the inflorescence protrudes from the</p><p>pseudostem the gametophyte or embryo sac has differentiated and the nuclei are in their</p><p>respective positions ready for fertilization (Fortescue and Turner, 2005b).</p><p>The development of the female flowers inside the pseudostem spans 12-13 weeks in the</p><p>tropics and is up to twice as long in the sub-tropics. Any effect of environmental conditions</p><p>during this time will be reflected in the shape and anatomy of the fruit. Morphological and</p><p>anatomical evidence suggests that the development of the flower in banana is sensitive to low</p><p>temperature when the ovary is differentiating (Fahn et al., 1961), when the perianth and</p><p>stamens are forming (White, 1928) and when the megasporangium is differentiating</p><p>(Fortescue and Turner, 2005a). These studies have been conducted mainly on triploid AAA</p><p>clones of the Cavendish subgroup. Low temperature when the ovary is differentiating is</p><p>associated with deformed fruit that are not suitable for marketing. Internally these fruits are</p><p>characterized by a reduced number of locules in the ovaries and in some flowers there are no</p><p>locules at all. Flowers with reduced locules develop into undersized fruit while those with no</p><p>locules form very small fruit no larger than the ovaries of neuter or male flowers (Fahn et al.,</p><p>1961).</p><p>Cool temperatures at the time of megasporogenesis and embryo sac formation can lead to</p><p>malformations in the ovule itself. Low temperature (3-18˚C) reduced the size of ovules and</p><p>caused them to have a rounder shape than normal ovules. In addition, the nucellus and</p><p>nucellar cap protruded through the micropyle. These deformations were observed in ovules in</p><p>bunches growing in the autumn, winter and spring in the subtropics. Fortescue and Turner</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>30</p><p>(2005a) suggested that megasporangium formation was particularly sensitive to low</p><p>temperature and that low temperatures need not last for more than a night or two.</p><p>There are three critical times in the reproductive biology of Musa when it is sensitive to</p><p>damage by low temperature. Firstly, low temperature affects the differentiation of the ovaries</p><p>and associated tissues soon after floral initiation. Secondly it affects the ovaries, when the</p><p>carpels and stamens are forming midway up the pseudostem. Thirdly, it affects the</p><p>differentiation of the megasporangium three to six weeks before anthesis.</p><p>Fruit Growth and Soil Water Deficit</p><p>Mahouachi (2008), in a field study on cv. ‘Grand Nain’ (AAA, Cavendish subgroup),</p><p>examined the effects of soil water deficit on the growth and nutrient concentrations of fruit</p><p>during the first two months after bunching, when the plants were re-watered, and then for a</p><p>further three weeks. Soil water content at 15 cm depth and 40 cm from the irrigation drip line</p><p>decreased exponentially with time from 33 to 15% during 63 d of drying. Upon re-watering,</p><p>the soil water content did not increase instantaneously, but increased linearly and reached</p><p>field capacity 20 d later. From the data of Mahouachi (2008) we calculated the effects of the</p><p>soil water deficit on rates of fruit growth and rates of accumulation of K in the fruit. In well-</p><p>watered plots the fruit grew (fresh and dry weights) exponentially for the 83 d of</p><p>measurement. For the first 63 d the relative growth rate (fresh weight) was 1.1% per day and</p><p>in the last 20 d it increased to 1.6% per day. This pattern of growth was similar in the fruit on</p><p>plants subjected to soil drying, but soil drying reduced the rate by 30% during soil drying (0-</p><p>63 d) and by 11% during re-watering (63-83 d). The fruit was still growing after 63 d of</p><p>drying. The net photosynthesis of the leaves had been reduced by 80% at this time. Soil water</p><p>deficit reduced the rates of accumulation of fresh weight and dry weight by 39% and the</p><p>accumulation of K by 57%. Soil drying reduced the accumulation of water and K in the fruit</p><p>and the K concentration fell by 19%, from 186 to 151 mmol K per “cell sap” volume. Re-</p><p>watering fully restored the rate of K uptake by the fruit but the accumulation of dry matter</p><p>was 17% less than control and the fresh weight was 30% less. These data suggest that the fruit</p><p>adjusts its growth rate to the supply of water available and that some of this adjustment may</p><p>be related to maintaining a sufficient concentration of K in the fruit tissues. This mechanism</p><p>allows the fruit to increase its absolute growth rate and complete its development, despite</p><p>dwindling supplies of water. Commercially, soil drying reduces fruit size, which is often a</p><p>criterion of quality for markets, and this effect begins soon after soil drying commences.</p><p>Nonetheless, the fruit continues to grow, albeit at a slower rate, whereas in a similar situation,</p><p>the emerging leaves on vegetative plants are likely to stop elongating. For fruit to grow as the</p><p>soil dries it must be able to attract water by having a more negative Ψw than other organs of</p><p>the plant. This might be achieved by decreasing its osmotic potential through the</p><p>accumulation of solutes. Since soil drying reduced the amount of K entering the fruit in the</p><p>experiment of Mahouachi (2008), any decrease in osmotic potential is not caused by K and</p><p>must be attributed to other osmolytes, perhaps sugars.</p><p>Bananas: Environment and Crop Physiology</p><p>31</p><p>CONCLUSION</p><p>Physiology is about how things work. We can also put physiology to work to improve</p><p>management and productivity of one of the world’s most important crops, the bananas. Much</p><p>of the research on physiology has been on a narrow group of cultivars (Cavendish subgroup,</p><p>AAA genome) that are currently important for the international trade. There is a need to</p><p>expand our interests to establish genotypic variation in physiological responses of the bananas</p><p>to the environment. For this work we can build on what is known about the Cavendish</p><p>subgroup as well as our knowledge of plant science, aspects of which we have considered in</p><p>this chapter. Steady progress is being made and the foundations for this work have been laid</p><p>in studies of the genetic diversity within Musa spp., briefly reviewed by Heslop-Harrison and</p><p>Schwarzacher (2007). The triploid nature of many cultivars, their parthenocarpy and sterility</p><p>have slowed genetic improvement in this crop species compared with other plants important</p><p>for human sustenance. Complementary progress in bananas might be made if physiological</p><p>knowledge was applied to the cultural techniques used to manage different cultivars in a</p><p>range of environments. The question then becomes: how can we best match the cultivar with</p><p>the environment to meet market requirements? Musa spp. are difficult to manage in</p><p>experiments partly because of their size. Nonetheless, we need to take up the challenge of</p><p>using more experimental manipulation to discover physiological mechanisms, rather than</p><p>relying on the correlative studies that are the basis of much of our current beliefs and</p><p>knowledge. We lack knowledge of environmental controls on the reproductive system and the</p><p>functional aspects of the root system. Exploring the physiology of a group of plants as</p><p>fascinating as the bananas is imperative. For those who take up the challenge, the work will</p><p>be intellectually satisfying and productive, perhaps mixed with a little frustration.</p><p>ACKNOWLEDGMENTS</p><p>We are grateful to colleagues for discussion of issues raised in this chapter.</p><p>REFERENCES</p><p>Aguilar EA, Turner DW, Sivasithamparam K. 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Regulation of floral initiation in horticultural trees. J. Exp.</p><p>Bot. 2008;59:3215-28.</p><p>In: Ecophysiology of Tropical Tree Crops ISBN 978-1-60876-392-4</p><p>Editor: Fabio DaMatta © 2010 Nova Science Publishers, Inc.</p><p>Chapter 3</p><p>CACAO: ECOPHYSIOLOGY OF GROWTH AND</p><p>PRODUCTION</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>ABSTRACT</p><p>Cacao (Theobroma cacao L.), one of the world’s most important perennial crops, is</p><p>almost exclusively explored for chocolate manufacturing. Most cacao varieties belong to</p><p>three groups: Criollo, Forastero and Trinitario that vary according to morphology, genetic</p><p>and geographical origins. Cacao is cropped under the shade of forest trees or as an</p><p>unshaded monocrop. Seedlings initially show an orthotropic growth with leaf emission</p><p>relatively independent of climate. The mature phase begins with the emission of</p><p>plagiotropic branches that form the tree crown. At this stage environmental factors exert a</p><p>large influence on plant development. Growth and development of cacao are highly</p><p>dependent on temperature, which mainly affects vegetative growth, flowering and fruit</p><p>development. Soil flooding decreases leaf area, stomatal conductance and photosynthetic</p><p>rates in addition to inducing formation of lenticels and adventitious roots. For most</p><p>genotypes drought resistance is associated with osmotic adjustment. Cacao produces</p><p>caulescent flowers, which begin dehiscing in late afternoon and are completely open at</p><p>the beginning of the following morning releasing pollen to a receptive stigma. Non-</p><p>pollinated flowers abscise 24-36 h after anthesis. The percentage of flowers setting pods</p><p>ranges from 0.5 to 5%. The most important parameters determinants of yield are related</p><p>to: (i) light interception, photosynthesis and capacity of photoassimilate distribution, (ii)</p><p>maintenance respiration, and (iii) pod morphology and seed formation. These events can</p><p>be modified by abiotic factors. Cacao is a shade tolerant species, in which appropriate</p><p>shading leads to relatively high photosynthetic rates, growth and seed yield. However,</p><p>heavy shade reduces seed yield and increases incidence of diseases. In fact, cacao yields</p><p>and light interception are highly correlated when nutrient availability is not limiting. High</p><p>production of unshaded cacao requires large inputs for protection and nutrition of the</p><p>crop. Annual radiation and rainfall during the dry season explains 70% of the variation in</p><p>annual seed yields.</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>38</p><p>INTRODUCTION</p><p>Cacao is a preferentially alogamous tropical woody species formerly in the Sterculiaceae</p><p>family (Cuatrecasas, 1964) and reclassified in the Malvaceae family (Alverson et al., 1999).</p><p>Under natural conditions the tree can reach 20 to 25 m in height (Lachenaud et al., 1997),</p><p>whereas under cultivation height varies from 3 to 5 m. The geographical origin of cacao is</p><p>South America (Motamayor et al., 2002), where several wild populations can be found in the</p><p>Amazon and Guyanian regions. It is considered one of the most important perennial crops on</p><p>the planet, with an estimated world output of 3.46 million tons in 2008/2009 (ICCO, 2009).</p><p>Cacao is predominantly grown in the tropical areas of Central and South America, Asia and</p><p>Africa (Marita et al., 2001) and is commercially exploited for seed output that is mainly</p><p>destined for chocolate manufacturing. However, derivatives and byproducts of cacao are also</p><p>transformed into cosmetics, fine beverages, jellies, ice creams and juices.</p><p>Traditionally cacao varieties in cropping systems belong to three main groups named</p><p>Criollo, Forastero and Trinitario, which differ according to morphology and genetic</p><p>characteristics and geographical origins (Bartley, 2005). Cacao Criollo was the first</p><p>domesticated cacao and has been cultivated for at least two millennia in Central and South</p><p>America (Sounigo et al., 2003). This group comprises varieties that produce fruits (pods)</p><p>containing white or pinkish seeds that yield seeds highly prized for their flavor and mainly</p><p>used in fine chocolates manufacture (Marita et al., 2001). Cacao Criollo is, however,</p><p>infrequently cultivated because of its high susceptibility to diseases (Soria, 1970). Varieties of</p><p>the Forastero group are widely cropped due to their high yields and resistance to diseases.</p><p>They produce around 80% of the world output of cacao seeds (Marita et al., 2001). This</p><p>group is subdivided into Lower and Upper Amazonian Forasteros; the former are cultivated in</p><p>the Amazon Basin and their cultivars were the first to be introduced in Africa, while the latter</p><p>are considered more genetically diversified and frequently used in breeding programs due to</p><p>their vigor, precocity and disease resistance (Iwaro et al., 2001). The first Forastero varieties</p><p>originated from the lower Amazon Basin and were cultivated mainly in Brazil and Venezuela</p><p>(Sounigo et al., 2003). The Trinitario group is considered a recent hybrid that originated from</p><p>crosses between Criollos and Lower Amazonian Forastero genotypes or intermediate types</p><p>(Motamayor, 2001).</p><p>Traditionally, cacao is cultivated under the shade of a selectively thinned forest (Lobão et</p><p>al., 2007) and represents one of the first agroforestry systems in tropical America. Cacao</p><p>agroforestry has been known since pre-Colombians times by the Mayas (Bergman, 1969). In</p><p>the Atlantic coastal forests of the states of Bahia and Espirito Santo, Brazil, around 4% of the</p><p>world and 75% of the Brazilian cacao output is obtained using a system locally called</p><p>Cabruca (Lobão et al., 2007). This system is a special kind of agroforestry in which the</p><p>understorey is drastically suppressed to introduce cacao, and the density of upperstorey trees</p><p>is reduced (Lobão et al., 2007). Cacao cultivation in this form shows much of the</p><p>sustainability attributes of the natural heterogeneous forest and is considered an efficient</p><p>agroforestry system (Figure 1) for protection of tropical soils against degradation agents</p><p>(Alvim, 1989b).</p><p>Cacao is also intercropped around the world in planned systems with other species of</p><p>economic value like Areca catechu, Cocos nucifera (Liyanage, 1985; Alvim and Nair, 1986;</p><p>Daswir and Dja’far, 1988; Abbas and Dja'far, 1989), Hevea brasiliensis, Syzigium</p><p>Cacao: Ecophysiology of Growth and Production</p><p>39</p><p>aromaticum, Cinnamomum zeylanicum, Erythrina fusca (Alvim, 1989a; 1989b), Bactris</p><p>gasipaes (Almeida et al., 2002a) and other Amazonian species (Brito et al., 2002). Several</p><p>agroforestry systems use more than three species in planned associations (Müller and Gama</p><p>Rodrigues, 2007). In contrast, cacao is also cropped under unshaded conditions (Figure 1). In</p><p>Ghana and Ivory Coast, for example, 50% of the total cacao farm area is under mild shade</p><p>whilst an average of 10% in Ghana and 35% in Ivory Coast is managed under no shade (Padi</p><p>and Owusu, 1998). In a shade and fertilizer trial conducted with Amazon cacao over a 20-</p><p>year period in Ghana, yield of heavily shaded plots was about half that under the non-shade</p><p>treatment (Ahenkorah et al., 1987). Despite this, the authors inferred that the economic life of</p><p>an unshaded Amelonado cacao farm in Ghana might not last for more than 15 years of</p><p>intensive cropping. Nonetheless, cacao can be produced economically with no shade if</p><p>adequate management practices including water and nutrient replenishment are utilized.</p><p>Figure 1. Some systems of cacao cropping: Cabruca, rubber x cacao and cacao without shade tree</p><p>(from left to right). Photos by the authors.</p><p>In this chapter, we provide information about the effects</p><p>of biotic and abiotic factors on</p><p>growth and development of the cacao plant that could be useful in the design of strategies for</p><p>new cropping systems. This is particularly important when also considering that the cacao</p><p>planting frontiers are being expanded towards marginal lands in tropical and subtropical</p><p>areas.</p><p>EFFECTS OF ABIOTIC FACTORS ON SEEDLING GROWTH AND</p><p>DEVELOPMENT</p><p>Cacao exhibits a considerable genetic variability in morphological and physiological</p><p>traits (Daymond et al., 2002a, 2002b). When it is multiplied via seeds, the seedling initially</p><p>displays an orthotropic growth pattern and exhibits repeated cycles of leaf flushes with spiral</p><p>phyllotaxy (Vogel, 1975). Furthermore, leaf emission occurs in a rhythmic way relatively</p><p>independent of climate, suggesting that growth rhythm is under endogenous control (Vogel,</p><p>1975). However, after achieving approximately 1.0 to 1.2 m in height, the orthotropic growth</p><p>ceases and the plant emits plagiotropic branches (Garcia and Nicolella, 1985). The number of</p><p>plagiotropic branches varies from three to five, forming what is generally named the cup or</p><p>crown of the cacao tree (Cuatrecasas, 1964). Also, there are inter- and intra-specific variations</p><p>for the orthotropic growth pattern (Batista and Alvim, 1981; Garcia and Nicolella, 1985). In</p><p>contrast to Soria (1964) and Garcia and Nicolella (1985), Batista and Alvim (1981)</p><p>demonstrated that the genetic background of orthotropic growth is influenced by</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>40</p><p>environmental factors. Environmental factors exert an influence of approximately 70% on the</p><p>development of the cacao plant at this stage (Garcia, 1973).</p><p>According to Greathouse et al. (1971) and Orchard et al. (1980), the specific stages of</p><p>leaf flushing in the orthotropic growth phase are: F-1 - bud swelling: leaf initiation and</p><p>unfolding; F-2 - leaf expansion: thin leaves, with strong anthocyanin pigmentation and apical</p><p>bud dormant; I-1 - leaf expansion complete: rapid greening and apical bud dormant; I-2 -</p><p>entirely expanded dark green leaves: apical bud dormant. Immediately after the emergence of</p><p>the next leaf, leaves in the initial F-1 stage are red and are positioned almost vertically</p><p>upwards. However, with expansion (F-2 stage) the stem:petiole angle decreases to</p><p>approximately 90° such that the petiole remains horizontal and, with an angle of</p><p>approximately 90° between the leaf blade and petiole, the blade hangs vertically downwards</p><p>(Abo-Hamed et al., 1983). During the F-2 stage the leaves are very thin and flexible. This</p><p>condition is maintained during leaf expansion until they enter the period of fast greening</p><p>(beginning of stage I-1), when the stem:petiole and leaf:petiole angles increase. Up to the</p><p>moment that the leaf blade becomes completely green, it thickens and becomes rigid with a</p><p>pronounced cuticle, and both the stem:petiole and leaf blade:petiole angles increase resulting</p><p>in the petiole and blade being positioned almost vertically. Subsequently the petiole:leaf blade</p><p>angle decreases approximately 90° and the blade is positioned horizontally (lower leaves).</p><p>This position is maintained until leaf senescence (Abo-Hamed et al., 1983).</p><p>Although the duration of the several stages of the flush cycle may vary depending on the</p><p>growth conditions [cf., for example, Greathouse et al. (1971) and Vogel (1975)] the basic</p><p>development pattern is relatively fixed, that is, the beginning of the cycle is marked by</p><p>swelling of the apical bud followed by unfolding of all leaves in the flush (Abo-Hamed et al.,</p><p>1983). The end of leaf production and the growth limitation of subsequent leaves within a</p><p>flush, which are smaller in size, are probably consequences of carbohydrate limitations, as</p><p>noted by Machado and Hardwick (1988b). They proposed that a new flush occurs following</p><p>an interflush period in which the carbohydrate supply is replenished; with the return of a</p><p>favorable carbohydrate balance a new leaf flush takes place.</p><p>According to Baker et al. (1975), (i) plastid length, breadth, number of grana and lamella</p><p>index per plastid, as well as the number of lamella per granum, increase with chlorophyll</p><p>(Chl) content; (ii) the number of chloroplasts per cell remains constant (three) during leaf</p><p>development; (iii) lutein, neoxanthin, violaxanthin, α- and β-carotenes are the carotenoids</p><p>found in measurable quantities in leaves; (iii) α-carotene is present in slightly higher</p><p>quantities than β-carotene; (iv) both xanthophylls and carotenes increase linearly with Chl</p><p>content during leaf development; and (v) the phase of maximum chloroplast development</p><p>occurs after the end of leaf expansion. Baker and Hardwick (1973) did not observe changes in</p><p>the molar relation of Chl a:b. However, Baker and Hardwick (1974) and Baker et al. (1975)</p><p>observed that (i) the photosynthetic capacity and the Chl content increased in parallel during</p><p>flushing; (ii) the maximum photosynthetic capacity per Chl unit remains constant during</p><p>chloroplast development; (iii) the saturating irradiance (Is) increases with increasing Chl</p><p>content; (iv) the total number of photosynthetic units increases one by one during leaf growth;</p><p>(iv) the photosynthetic efficiency increases per Chl unit during leaf development; (v) the</p><p>thylakoid formation occurs in parallel with Chl synthesis during chloroplast development; (vi)</p><p>the maximum phase of chloroplast development may not occur until after the end of leaf</p><p>expansion; (vii) the phase of maximum synthesis of Chl coincides with the end of the linear</p><p>phase of leaf expansion; (viii) Rubisco activity increases with the content of Chl and can be a</p><p>Cacao: Ecophysiology of Growth and Production</p><p>41</p><p>limiting factor for photosynthesis; and (ix) the Chl content can be used as a general indicator</p><p>of chloroplast development.</p><p>The apparent absence of green pigmentation in young cacao leaves is not related to the</p><p>delay in chloroplast development, but is due to the fact that chloroplasts are initially very</p><p>small and usually few (Whatley, 1992). The delay in greening of leaves is associated with a</p><p>late increase in the total extension of the thylakoid system inside each cell that accompanies</p><p>the subsequent increase in plastid size (Whatley, 1992). Lee et al. (1987) reported that the</p><p>changes in color shown by cacao leaves during its ontogeny resulted from varying levels of</p><p>different pigments, like anthocyanins and/or phenols, which initially mask the Chl content</p><p>(Figure 2). Content of these pigments fluctuates during leaf expansion (total content of</p><p>phenols remains high and that of anthocyanins decreases with maturity).</p><p>On the hypostomatous cacao leaf surface (Hardwick et al., 1981) four main kinds of hairs</p><p>are found, the most common of which are thick and short, with a multicellular rounded head</p><p>(Abo-Hamed et al., 1983). In 4-d-old leaves, stomata are found only in the midribs, primary</p><p>lateral and minor veins; however, only those of the midribs are completely developed and can</p><p>open. Stomata of the secondary and lateral ribs open within 2-4 d, and those in inter-veinal</p><p>regions begin to develop and can open towards the end of the leaf expansion phase (Abo-</p><p>Hamed et al., 1983). According to Abo-Hamed et al. (1983) the maturation of stomata is</p><p>correlated with the presence of Chl. The cuticle thickness increases at a constant rate during</p><p>leaf expansion and achieves maximum thickness during the I-1 stage. Additionally, stomata</p><p>and cuticle development follow a pattern closely correlated with the growth stages of the leaf.</p><p>Figure 2. Seedling flushing in the field and details of a flush. Note the color variability in the seedling</p><p>leaves. Photos by the authors.</p><p>Solar Radiation</p><p>Müller et al. (1992), evaluating photosynthesis in cacao leaves of different ages grown</p><p>under two irradiances, found a strong effect of light intensity during leaf development on</p><p>photosynthetic capacity of mature leaves. In cacao, shade leaves often</p><p>species such as banana, cassava, citrus,</p><p>cocoa, coconut, coffee, mango, oil palm, papaya, rubber, and tea.</p><p>This book is based to a large extent on review articles published in a special issue of the</p><p>Brazilian Journal of Plant Physiology (volume 19, issue 4, 2007). Most of these articles were</p><p>written by leading investigators from Asia, Australia, Europe, South America, and United</p><p>States that were invited by myself when I was the Editor-in-Chief of that journal. Following</p><p>that special issue, there is a great deal of pliancy in the orientation, deepness and style of each</p><p>chapter of the present volume. In fact, the authors’ contributions reflect to a large extent their</p><p>particular research specialties with tree crops grown in tropical and subtropical regions.</p><p>Overall, the book will hopefully serve as a stimulus for further effort in the challenging field</p><p>of environmental physiology research.</p><p>I thank the National Council for Scientific and Technological Development (CNPq,</p><p>Brazil), the Brazilian Consortium for Coffee Research and Development, and the Foundation</p><p>for Research Assistance of the Minas Gerais State (Fapemig, Brazil) for the continuous</p><p>financial support of my research projects throughout recent years. I thank all those have</p><p>contributed in many different ways to the production of this book, particularly the authors of</p><p>the chapters for their patience and kind cooperation during the production process. I am</p><p>thankful to Ms. Gilmara M. Pompelli and my Master’s student Samuel Cordeiro V. Martins</p><p>for their invaluable assistance re-editing many of the tables, graphs and photographs</p><p>published here. I am also grateful for the sincere collaboration I received from my friend</p><p>Professor Raimundo S. Barros, for his encouragement in editing this book and for his</p><p>painstaking corrections of my English during the preparation of this volume. A kind</p><p>acknowledgment is also made of the permissions granted by journals’ and books’ publishers</p><p>for the reproduction of graphs and tables as acknowledged in the respective captions.</p><p>Fábio M. DaMatta x</p><p>Last, but not least, I wish to express a debt of gratitude to the Editorial Board of the Brazilian</p><p>Society of Plant Physiology for allowing me to use the special issue mentioned above to</p><p>publish this volume.</p><p>June 2009</p><p>Fábio M. DaMatta</p><p>ABBREVIATIONS</p><p>A rate of net CO2 assimilation</p><p>ABA abscisic acid</p><p>ACC 1-aminocyclopropane-1-carboxylic acid</p><p>Ag rate of gross CO2 assimilation</p><p>A/gs intrinsic water-use efficiency</p><p>AM arbuscular mycorrhizal</p><p>Am maximum rate of net CO2 assimilation</p><p>Amax light-saturated rate of net CO2 assimilation</p><p>AP1 APETALA1</p><p>a.s.l. above sea level</p><p>ASW available soil water</p><p>AtCO Arabidopsis CONSTANS gene</p><p>AZ abscission zone</p><p>BBP bunch biomass production</p><p>BG bunch growth</p><p>BGD ‘Brazilian Green Dwarf’</p><p>BI bunch index</p><p>Ca atmospheric or ambient CO2 concentration</p><p>Chl chlorophyll</p><p>Ci intercellular CO2 concentration</p><p>CIAT International Center for Tropical Agriculture</p><p>CIMMYT International Maize and Wheat Improvement Center</p><p>CNPMF Centro Nacional de Pesquisa em Mandioca e Fruticultura</p><p>CO CONSTANS</p><p>Cp mass specific heat of air</p><p>CPR crop performance ratio</p><p>DAC daily gross photosynthetic integral of a crop canopy</p><p>DM dry mass; also dry matter</p><p>DMP dry matter production</p><p>DNA deoxyribonucleic acid</p><p>DW dry weight</p><p>E transpiration rate</p><p>e radiation conversion efficiency</p><p>e* energy-adjusted radiation conversion efficiency</p><p>Fábio M. DaMatta</p><p>xii</p><p>EE transpiration efficiency</p><p>EMBRAPA Empresa Brasileira de Pesquisa Agropecuária</p><p>ET evapotranspiration</p><p>FD transcription factor</p><p>FFB fresh fruit bunches</p><p>FM fresh mass; also fresh matter</p><p>FP florigenic promoter</p><p>FS filtered shade</p><p>FT FLOWERING LOCUS T</p><p>Fv/Fm variable-to-maximum chlorophyll fluorescence ratio</p><p>FW fresh weight</p><p>GA gibberellin</p><p>GA3 gibberellic acid</p><p>GABA γ-aminobutyrate</p><p>gb boundary layer conductance</p><p>GDD growing-degree-days</p><p>gm mesophyll conductance</p><p>gp whole-plant hydraulic conductance</p><p>gs stomatal conductance; also diffusive conductance</p><p>h day length</p><p>HCN hydrocyanic acid</p><p>HI harvest index</p><p>HL high sunlight</p><p>HN high nitrogen</p><p>I irradiance</p><p>IAA indole-3- acetic acid</p><p>Ic light compensation point</p><p>Id daily light integral</p><p>IITA International Institute of Tropical Agriculture</p><p>IRGA infra-red gas analyzer</p><p>IRRI International Rice Research Institute</p><p>Is saturating irradiance; also light saturation point</p><p>J rate of photosynthetic electron transport</p><p>JA jasmonic acid</p><p>Jmax light-saturated rate of photosynthetic electron transport</p><p>K Granier heat coefficient</p><p>k light extinction coefficient</p><p>LAI leaf area index</p><p>LER land equivalent ratio</p><p>Lm mesophyll limitation</p><p>LN leaf nitrogen content; also low nitrogen</p><p>LRC light response curve</p><p>LS relative stomatal limitation</p><p>LSD least significant difference</p><p>Ma mass-to-area ratio</p><p>MACC malonyl-ACC</p><p>Abbreviations</p><p>xiii</p><p>MDP midday depression of photosynthesis</p><p>MiCOL CONSTANS-like gene</p><p>MRD ‘Malayan Red Dwarf’</p><p>MYD ‘Malayan Yellow Dwarf’</p><p>na not available</p><p>Na nitrogen concentration per area basis</p><p>NADP-IDH NADP(+)-isocitrate dehydrogenase</p><p>Nm nitrogen concentration per mass basis</p><p>NN no nitrogen</p><p>NS neutral shade; also non significant</p><p>Nsh number of plucked shoots per unit land area</p><p>O/B palm oil- to-bunch ratio</p><p>P probability level; also fraction of dry matter partitioned to bunches</p><p>PAR photosynthetically active radiation</p><p>PDD penalized degree-days</p><p>PEPC phosphoenolpyruvate carboxylase</p><p>PET potential evapotranspiration</p><p>PKO palm kernel oil</p><p>PNUE photosynthetic nitrogen-use efficiency</p><p>PO palm oil</p><p>PPFD photosynthetic photon flux density</p><p>PRD partial root zone drying</p><p>PSII photosystem II</p><p>QE quantum efficiency</p><p>qN non-photochemical quenching coefficient</p><p>qp photochemical quenching coefficient</p><p>R intercepted radiation</p><p>ra aerodynamic resistance</p><p>rc canopy resistance</p><p>Rd day respiration rate; also dark respiration rate</p><p>RH relative humidity</p><p>rs stomatal resistance</p><p>RSL relative stomatal limitation</p><p>Rubisco ribulose-1,5-bisphosphate carboxylase/oxygenase</p><p>RUBP ribulose-1,5-bisphosphate</p><p>RUE radiation-use efficiency</p><p>R-V reproductive-to-vegetative</p><p>RWC relative water content</p><p>S incident solar radiation</p><p>Sc fraction of S amount intercepted by the canopy</p><p>SE standard error</p><p>SER shoot extension rate</p><p>SOM soil organic matter</p><p>SRC shoot replacement cycle</p><p>SWC soil water content</p><p>SWD soil water deficit</p><p>Fábio M. DaMatta</p><p>xiv</p><p>T transpiration</p><p>t ton</p><p>Ta air temperature</p><p>Tb base temperature</p><p>TBP total biomass production</p><p>Tc canopy temperature</p><p>Tce ceiling temperature</p><p>TDMP total dry matter production</p><p>TL leaf temperature</p><p>TNCa total non-structural carbohydrates per unit leaf area</p><p>To optimum temperature</p><p>TPU triose phosphate use</p><p>Ts soil temperature</p><p>TSS total soluble solids</p><p>u wind speed</p><p>UGD ‘Brazilian Green Dwarf from Una’</p><p>VAM vesicular-arbuscular mycorrhizal fungi</p><p>VBP vegetative biomass production</p><p>Vcmax maximum carboxylation rate allowed by Rubisco</p><p>VG vegetative growth</p><p>VP vegetative promoter</p><p>VPD vapor pressure deficit</p><p>V-R vegetative-to-reproductive</p><p>Wsh mean weight per shoot</p><p>WUE water-use efficiency</p><p>Y yield</p><p>γ psychrometric constant</p><p>ε bulk modulus of elasticity</p><p>θ convexity of the irradiance response curve</p><p>Δ slope of the curve</p><p>λ latent heat of vaporization</p><p>ρ density of air</p><p>Φapp apparent quantum yield</p><p>ΦEXC efficiency of PSII in capturing actinic light</p><p>Ψs osmotic potential</p><p>Ψw water potential</p><p>In: Ecophysiology of Tropical Tree Crops ISBN 978-1-60876-392-4</p><p>Editor: Fabio DaMatta © 2010 Nova Science Publishers, Inc.</p><p>Chapter 1</p><p>INTRODUCTION</p><p>Fábio M. DaMatta</p><p>Plant physiological research has a fundamental role in advancing our understanding of</p><p>exhibit greater total</p><p>Chl concentrations per unit mass than sun leaves (Merkel et al., 1994). Ontogenetic changes</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>42</p><p>in the leaf Chl a:b ratio is a controversial issue, as it has been shown to increase continuously</p><p>(Merkel et al., 1994) or to be held in check (Baker and Hardwick, 1973, 1974) during leaf</p><p>development. Costa et al. (1998), evaluating the growth of cacao seedlings under different</p><p>light levels and N concentrations, verified increases in leaf lamina thickness positively</p><p>correlated with the increase of light intensity, independent of N concentration. Under shade</p><p>conditions and high N concentrations, they observed that the spongy parenchyma had a</p><p>reduced number of small cells distributed over vast intercellular spaces, while short cells</p><p>constituted the palisade parenchyma, interspersed by quite large spaces.</p><p>Seedlings grow slowly under full sunlight and some degree of shade is beneficial for their</p><p>establishment (Okali and Owusu, 1975). Thus, shelter trees have been invariably</p><p>recommended for the establishment of cacao seedlings (Alvim, 1977), which would be</p><p>gradually removed with increasing self-shade (Byrne, 1972). The slow growth of seedlings</p><p>under full sunlight is due to constraints on leaf expansion, which is most likely caused by</p><p>excessive transpiration that would induce leaf water stress (Okali and Owusu, 1975). In</p><p>contrast, shaded leaves show higher relative water content and fewer stomata per unit leaf</p><p>area than unshaded leaves. The perpendicular positioning of young leaves in the flush, the</p><p>presence of superficial hairs, the rapid synthesis of cuticle and the development of stomata,</p><p>which are all limited to the initial stages of leaf expansion, act to reduce the water loss of</p><p>developing leaves (Abo-Hamed et al., 1983).</p><p>The saturating irradiance for photosynthesis of a mature cacao leaf varies from 6%</p><p>(Baker and Hardwick, 1973) to 30% (Okali and Owusu, 1975) of full sunlight, while for a</p><p>developing leaf Is increases with increasing Chl content (Baker and Hardwick, 1976). At Is,</p><p>younger leaves (PF1) in the flush showed photosynthetic rates significantly higher than those</p><p>from both the oldest leaves of PF2 (middle age leaves) and PF3 (old leaves) (Machado and</p><p>Hardwick, 1988a). Under field conditions, the total potential contribution of photosynthesis</p><p>of the oldest leaves would be remarkably reduced as a consequence of mutual shading in the</p><p>crown interior (Machado and Hardwick, 1988b).</p><p>Cacao seedlings show increasing rates of net CO2 assimilation (A) as the</p><p>photosynthetically active radiation (PAR) increases to values in the range from near 400</p><p>(Joly, 1988) to 750 (Da Matta et al., 2001) µmol m-2 s-1, which corresponds to 20 to 35% of</p><p>PAR at full sunlight, when Is is reached. About 95% of the maximum A is obtained with half</p><p>Is. At full sunlight, A declines at light exposures above 30% of the global radiation (Okali and</p><p>Owusu, 1975; Hutcheon, 1976), in which A of many plant species usually peaks (Alvim,</p><p>1965). Baligar et al. (2008), measuring A in three cacao clones, showed that increasing PAR</p><p>from 50 to 400 µmol m–2 s–1 led to increases in A by about 50%, but further short-term</p><p>increases in PAR up to 1500 µmol m–2 s–1 had no effect on A.</p><p>For leaves developed under shade conditions, a decrease in A occurs below 20% of full</p><p>sunlight (Owusu, 1978), whereas Okali and Owusu (1975) found in shade leaves that Is</p><p>occurred at around 3-4% of full sunlight. Therefore, the varying Is should be a reflection of</p><p>differences in growth and measurement conditions.</p><p>Cunningham and Burridge (1960) by submitting cacao seedlings to full sunlight and</p><p>heavy shading (85%) showed that water and mineral nutrients were the most crucial factors</p><p>for growth promotion at full sunlight. According to Okali and Owusu (1975) nutrients may be</p><p>more important than shading for seedling establishment. Costa et al. (1998), by growing</p><p>cacao seedlings under different light levels and N doses, observed a significant increase in</p><p>Chl content of mature and more shaded leaves, especially at higher N doses. The increase at</p><p>Cacao: Ecophysiology of Growth and Production</p><p>43</p><p>all irradiances tested occurred in the presence of up to 10 mM of N, but above that Chl</p><p>concentration leveled off. Okali and Owusu (1975) and Merkel et al. (1994) found similar</p><p>results regardless of Chl content and PAR for other cacao genotypes.</p><p>For cacao plantation systems it is hypothesized that once the nutritional demands are met,</p><p>the yield of the understorey crop is dependent mainly on the accessibility to solar radiation</p><p>(Cunningham and Arnold, 1962). In any case, Hutcheon (1973) evaluating the growth of the</p><p>cacao clone Scavina-6 and two other Amelonado genotypes under full sunlight, verified that</p><p>the former is more tolerant to excessive radiation than the Amelonados. Scavina-6 kept more</p><p>leaves and grew well at full exposure, whereas the leaf area of Amelonado was halved,</p><p>showing that seedling capacity to grow under full sunlight is also related to genetic factors.</p><p>Temperature</p><p>Cacao growth and development, as also occur with other tropical woody species, is</p><p>highly dependent on temperature (Raja Harun and Hardwick, 1988b; Hadley et al., 1994).</p><p>This can be observed through the reduction of photosynthetic rates at temperatures above or</p><p>below the range considered optimal (Raja Harun and Hardwick, 1988b). Low temperatures</p><p>affect mainly vegetative growth (Alvim et al., 1977), flowering (Alvim, 1988) and fruit</p><p>development (Sale, 1969).</p><p>Daymond and Hadley (2004), evaluating the effect of temperature on the initial</p><p>vegetative growth, emission of Chl fluorescence and leaf Chl content in seedlings of four</p><p>cacao genotypes, showed the existence of genetic variability in response to temperature stress.</p><p>In a study by Amorim and Valle (1990), in which gas exchanges were measured on 8-month-</p><p>old cacao seedlings submitted to different root temperatures (10, 20, 30 and 40°C), it was</p><p>found that at root temperatures between 20 and 30°C the water fluxes and stomatal</p><p>conductance (gs) were greater than at any other soil temperature. Consequently, the resistance</p><p>to water movement was low and A rates were higher.</p><p>Daymond and Hadley (2004) calculated cacao base temperatures (temperatures below the</p><p>point at which development ceases) that varied from 18.6 to 20.8°C. These values are</p><p>considerably higher than those obtained by Alvim (1977), who calculated a base temperature</p><p>of 9°C for Catongo based in its pod growth ability. The higher base temperatures of</p><p>Daymond and Hadley (2004) were probably due to the fact that their studies were conducted</p><p>under conditions of low irradiance, while the studies by Alvim (1977) were carried out under</p><p>field conditions.</p><p>Okali and Owusu (1975) observed that leaf temperatures of unshaded cacao seedlings are</p><p>higher than that for shaded seedlings, and the transpiration rate (E) is usually at its maximum.</p><p>The vertical orientation of developing cacao leaves decreases light interception, and, thus,</p><p>leaves can be kept cooler and water loss may be limited in comparison to mature horizontally</p><p>positioned leaves (Abo-Hamed et al., 1983). Low Chl content and high anthocyanin</p><p>pigmentation of expanding leaves also contribute to maintain relatively low leaf temperature</p><p>and, together with the presence of relatively dense hair cover on the leaf surface, may</p><p>contribute to further decreased E (Abo-Hamed et al., 1983).</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>44</p><p>Relative Humidity</p><p>Stomatal opening in cacao leaves is related to the air relative humidity (RH) – stomata</p><p>are kept more open at higher than lower RH (Sena Gomes et al., 1987). However, due</p><p>probably to a high cuticular transpiration, stomatal closure does not always efficiently control</p><p>water loss. In fact, some cacao genotypes do not show high stomatal resistance under water</p><p>deficit and low RH (Raja Harun and Hardwick, 1988). This is</p><p>in contrast to other genotypes</p><p>where an efficient mechanism of stomatal regulation may strongly limit E under water deficit</p><p>conditions. This may be an important acclimation strategy against drought (Balasimha, 1988).</p><p>In fact, the extreme sensitivity of some cacao genotypes to low RH can be a limiting growth</p><p>factor in areas where RH is low (Sena Gomes et al., 1987). In such areas, growth may be</p><p>adversely affected as a result of stomatal closure and, consequently, a reduction of A is to be</p><p>expected. The inefficient use of water (low water-use efficiency, WUE = A/E) at low RH</p><p>probably would cause water deficit in shoots under limited soil water supply (Sena Gomes et</p><p>al., 1987). According to Baligar et al. (2008), increasing VPD leads to decreases in A with</p><p>parallel increases in E, thus ultimately lowering WUE. Furthermore, under the conditions of</p><p>their measurements, Baligar and co-workers showed an unusually poor response of gs to</p><p>VPD, which could limit the ability of cacao to grow where VPD is high. Nonetheless, high A</p><p>and high WUE of cacao in a high RH regime are consistent with many species of the humid</p><p>tropics (Alvim, 1977; Wood, 1985).</p><p>Water Supply</p><p>Both water excess (flooding) and water deficit impair cacao growth and development.</p><p>Flooding is an important barrier for the initial growth and establishment of cacao in places</p><p>subjected to periodic waterlogging. Waterlogging occurs in some cacao producing areas in</p><p>Brazil, Ghana, Nigeria and Ivory Coast, where total rainfall often largely exceeds</p><p>evapotranspiration, which creates hypoxic conditions in the soil (Sena Gomes and Kozlowski,</p><p>1986). In the state of Bahia, Brazil, the hypoxic condition occurs after heavy rainfalls in</p><p>locations with shallow soils, as well as areas with hydromorphic soils and margins of rivers</p><p>after periodic floods. Decreases in growth, leaf area, gs and A, as well as epinasty, leaf fall,</p><p>formation of hypertrophic lenticels and adventitious roots in submerged stems have been</p><p>found during the flooding period. The extent of these changes is genotype dependent (Rehem,</p><p>2006). Sena Gomes and Kozlowski (1986) reported similar results for cacao seedlings of</p><p>Catongo. Bertolde (2007) studying 35 cacao clones in the young phase found some tolerant</p><p>genotypes and demonstrated that there are no significant relationships among physiological</p><p>variables in response to flooding and heterozygosis patterns. In any case, growth inhibitions</p><p>in plants submitted to soil flooding reduce pod production due to the delay of flowering and</p><p>suppression of vegetative growth (Sena Gomes and Kozlowski, 1986). A similar result was</p><p>also found by Mariano and Monteiro (1980), who showed an approximately 60% reduction in</p><p>pod production after a flooding of some weeks.</p><p>Water deficit, in addition to impairing crop yield of adult plants, also negatively affects</p><p>growth of cacao seedlings. Almeida et al. (2002b) evaluated the effects of water stress in 5-</p><p>month-old seedlings of eight cacao genotypes grafted on the variety Cacau Comum. They</p><p>demonstrated that (i) drought resistance occurred, at least partially, through osmotic</p><p>Cacao: Ecophysiology of Growth and Production</p><p>45</p><p>adjustment in most genotypes; (ii) the genotypes maintained values of relative water content</p><p>at around 90% with a leaf water potential (Ψw) of approximately -1.0 MPa, gradually reaching</p><p>55% at -3.5 MPa; (iii) a significant increase occurred in leaf concentration of K and P during</p><p>the dehydration process of some genotypes at Ψw of -1.5 MPa.</p><p>In cacao, leaf carbon export rate is sharply reduced with the decline of Ψw between -0.8</p><p>and -2.0 MPa. This reduction is strictly associated with both A and the export capacity, which</p><p>is strongly reduced when A approaches zero (Deng et al., 1989). Deng et al. (1990) found</p><p>values of A close to zero at Ψw below -1.6 MPa, while average values of A of about 2.2 µmol</p><p>CO2 m-2 s-1 were found at approximately -1.5 MPa. This was also observed by Gama-</p><p>Rodrigues et al. (1995), who attributed to K fertilization a role in the mechanisms to reduce</p><p>the negative effects of severe water stress in cacao, independently of the K source.</p><p>Nutrients – K</p><p>Cacao requires large amounts of K, and approximately 700 kg ha-1 are necessary to</p><p>produce 1000 kg ha-1 of seeds per year (Thong and Ng, 1980). This element corresponds to</p><p>about 70% of the nutrients in the sap of the cacao xylem (Martins, 1976). Orchard (1978)</p><p>showed in cacao seedlings that high doses of K (5 mmol L-1) promoted increased leaf area</p><p>without affecting dry biomass production. He also showed that there is an inverse relationship</p><p>between leaf transpiration and K availability. Under field conditions cacao trees well supplied</p><p>with K may be more tolerant to the adverse effects of water stress (Bosshart and Uexkhull,</p><p>1987). According to Gama-Rodrigues et al. (1995), KCl was the K source that induced the</p><p>lowest gs, E and A, which differed significantly from the sources K2SO4 and Kalsilite. There</p><p>were no significant effects among K sources on WUE, Ψw and internal CO2 concentration.</p><p>The largest dose of K added to the soil, however, resulted in smaller values of A and larger</p><p>values of E, thus decreasing WUE but without affecting shoot dry biomass.</p><p>FINE ROOTS IN CACAO TREES</p><p>The capacity of a tree to absorb water and nutrients depends, among other factors, on fine</p><p>root dynamics (mortality rates and regrowth of fine roots) as well as its variation in time. The</p><p>turnover of fine roots can contribute a significant proportion of recycled nutrients in</p><p>agroforestry systems, where the competition between forest trees and crops for water and</p><p>nutrient depends on the temporal pattern of fine root regrowth (Muñoz and Beer, 2001).</p><p>Studies done under greenhouse conditions have shown that cacao seedlings, as with many</p><p>tropical woody species, have alternate phases of root and shoot growth (Taylor and Hadley</p><p>1987). Field evaluations of fine root growth in cacao trees have been very much limited to</p><p>static inventory data. For example Beer et al. (1990) assessed biomass only at a single</p><p>harvest. Although Kummerow et al. (1981, 1982) accomplished a pioneer study with cacao</p><p>root dynamics, their methodology involved sequential coring, which can lead to significant</p><p>over or underestimation of root productivity (Anderson and Ingram, 1993).</p><p>Biomass of active fine roots (≤ 2 mm at 0-10 cm soil depth) of 11-yr-old cacao plants</p><p>shaded by Erythrina glauca was reported as 0.8 Mg ha-1 (Kummerow et al., 1981) and 0.4</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>46</p><p>Mg ha-1 for roots ≤ 1 mm (Kummerow et al., 1982). In cacao plantations shaded by E.</p><p>poeppigiana or Cordia alliodora the biomass of cacao fine roots, on average, was</p><p>approximately 1.0 Mg ha-1 and changed little during the year (Muñoz and Beer, 2001). The</p><p>maximum value found at the beginning of the rainy season was 1.85 Mg ha-1 in the cacao-C.</p><p>alliodora system compared to 1.20 Mg ha-1 for cacao-E. poeppigiana. According to Muñoz</p><p>and Beer (2001), if the annual turnover of fine roots were constant and close to 1.0 Mg ha-1 in</p><p>both systems, the input of nutrients would be 23-24 (N), 2 (P), 14-16 (K), 7-11 (Ca) and 3-10</p><p>kg ha-1 yr-1, which would represent 6-13% and 3-6% respectively of the total input of</p><p>nutrients in the organic matter for the C. alliodora and E. poeppigiana systems.</p><p>Growth and longevity measurements of fine roots (diameter < 1 mm) performed by Silva</p><p>and Kummerow (1998) directly in the soil-litter interface, in a Brazilian cacao plantation</p><p>shaded with E. fusca, revealed that the elongation rates of fine roots were, on average, 3.7 and</p><p>1.8 mm d-1 for ramifications of first and second order, respectively. They also found that the</p><p>average period of functional life of these roots was 3 d, with a range of 1 to 10 d, and that</p><p>growth of fine roots was closely correlated with rain frequency. Data reported by Silva and</p><p>Kummerow (1998), Kummerow et al. (1982) and Medeiros et al.</p><p>(1987) suggest that life</p><p>spans of fine roots are short, but, in compensation, they have high turnover rates.</p><p>According to Muñoz and Beer (2001), the low fine root production between October and</p><p>January in Costa Rica is probably the result of internal distribution of carbon to pod</p><p>production during the six months that it takes for fruits, harvested in December-January, to</p><p>develop and mature. Furthermore, these authors reported that partial pruning of cacao in</p><p>December might also reduce cacao fine root production during the following months due to</p><p>reduction in photoassimilate production and internal competition between flushing and root</p><p>renewal (Muñoz and Beer, 2001). A negative correlation between number of new leaves per</p><p>flush and number of growing root tips was reported by Kummerow et al. (1982). The</p><p>observations of Muñoz and Beer (2001) in Costa Rica are consistent with observations in</p><p>Brazil that the number of active cacao root tips (0-10 cm soil depth) was lowest in the driest</p><p>month and highest in the wettest month (Kummerow et al., 1982). Therefore, this temporary</p><p>increase in fine root production seems to be part of the normal phenological cycle of cacao</p><p>(Muñoz and Beer, 2001) since formation of new root tips in cacao grown in nutrient solution</p><p>was reported only during the rainy month of July in Costa Rica (Rodriguez et al., 1963).</p><p>Additionally, the results regarding fine root dynamics of shaded cacao plantations suggest</p><p>that a greater proportion of nutrients in organic or inorganic fertilizers is absorbed by cacao at</p><p>the beginning, rather than at the end, of the rainy season (Muñoz and Beer, 2001).</p><p>Experiments (B.V. Leite, 2007; unpublished results) conducted with 35-month-old cacao</p><p>plants in a semi-arid region of Bahia, Brazil, in which irrigation was performed by placing</p><p>one or two plastic pipes at 0.30 m from the trunk with drip emitters 0.50 m apart, revealed</p><p>that in plants grown in plots with two irrigation pipes, the longitudinal root length (along the</p><p>planting line) was about 1.70 m and the perpendicular (to the planting line) root length was</p><p>about 1.0 m for both sides of the trunk. For the cacao plots with only one pipe the</p><p>longitudinal root length (along the planting line) was, on average, 2.0 m. Perpendicularly to</p><p>the planting line a clear root displacement towards the dripping pipe was observed. At the</p><p>opposite side, without a pipe, the roots were finer, fewer and smaller in length. Clearly, the</p><p>greater concentration of radicels was observed near the irrigation pipe. In the two-pipe plots</p><p>the tap roots reached a depth of 1.3 m against 1.0 m for the one pipe irrigation plot, indicating</p><p>that the growth limitation was due to the size of the wetted soil area (Figure 3).</p><p>Cacao: Ecophysiology of Growth and Production</p><p>47</p><p>Figure 3. Root system of cacao plants grown in plots with one (left) and two (right) irrigation pipe lines.</p><p>Note the skewed distribution of roots in the plant grown in plots irrigated with one pipe line. Photos by</p><p>the authors.</p><p>The wetted area, after 2 h of irrigation, reached 0.7 m in depth and 0.6 m diameter. In this</p><p>system 3% of the roots were concentrated between 0-0.1 m, 80% between 0.1 to 0.6 m, and</p><p>17% below 0.6 m depth. For the one-pipe plot the wetted area was 0.4 m in depth and 0.5 m</p><p>diameter after 2 h of irrigation. In this system 9% of the roots were distributed between 0-0.1</p><p>m, 56% between 0.1-0.4 m, and 35% below 0.5 m depth, and these were skewed to the side of</p><p>the irrigation pipe. The distribution of fine, medium and coarse roots followed the same</p><p>patterns, that is, in the two-pipe plots, they were distributed along the two sides of the pipes.</p><p>The fine roots were at a higher percentage while the medium and coarse roots presented about</p><p>the same percentage. In the one-pipe plots the percentage of fine roots was higher than</p><p>medium and coarse roots. However, fine roots were generally low in number as well as</p><p>distributed preferentially on the side of the irrigation pipe. From these preliminary results</p><p>(B.V. Leite, 2007, unpublished data) it can be concluded that the behavior of the plant as a</p><p>whole, and the root system in particular, is different from the traditional cropping areas in</p><p>which soil moisture depends on rainfall. In the traditional cacao growing areas the fine root</p><p>system is concentrated in the first 0.2 m soil depth, and most fine roots are located in the first</p><p>0.10 m (Leite and Cadima Zevallos, 1991).</p><p>THE FLUSHING CYCLE</p><p>Formation of a cacao branch is characterized by alternate periods of growth and</p><p>quiescence, i.e. the flush cycle (Greathouse et al., 1971). During flush activity a variable</p><p>number of leaves is produced in fast succession, after which the leaves rapidly expand (Baker</p><p>and Hardwick, 1973). Under field conditions, the flushing cycle is activated usually by</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>48</p><p>environmental changes (Almeida et al., 1987). However, the cycle persists under constant</p><p>conditions (Orchard et al., 1980) that indicates there is an endogenous form of control along</p><p>the flush cycle. Studies reported by Alvim et al. (1974b), Orchard et al. (1981) and Abo-</p><p>Hamed et al. (1981) showed that the alternating growth and quiescence periods of the apical</p><p>bud of the cacao branch (the flush cycle) is controlled by a regular cycle of accumulation and</p><p>depletion of growth promoter and inhibitor compounds in the bud. Instead of in situ synthesis,</p><p>transport of abscisic acid (ABA) (Alvim et al., 1974b) and cytokinins (Orchard et al., 1981)</p><p>towards the apical bud has been proposed.</p><p>Growth Promoters and Inhibitors</p><p>The highest levels of auxin and cytokinin are found in young, expanding cacao leaves of</p><p>a new flush (Orchard et al., 1981). This suggests that these leaves could be acting either as</p><p>sinks, importing auxin and cytokinins from other parts of the plant, or as auxin and cytokinin</p><p>sources, from where these promoters are exported to the apical bud and other plant parts. The</p><p>auxin and cytokinin levels in young leaves close to the apex could also reflect the increase in</p><p>transport of these compounds to the higher parts of the flush, including the apex (Abo-Hamed</p><p>et al., 1984).</p><p>Analyses of new and previous flushes of cacao plants under controlled environment</p><p>(Orchard et al., 1980) or under water deficit conditions (Alvim et al., 1974b) showed high leaf</p><p>levels of ABA when the apex is in the quiescence phase of the cycle. In agreement with the</p><p>distribution of [14C]ABA in cacao, it is suggested that ABA is exported from the leaf, via</p><p>phloem, to areas of low ABA concentrations such as buds and young leaves, which is</p><p>consistent with source/sink relationships. ABA induces branch quiescence or, alternatively,</p><p>helps to maintain the branch in the non-active state. Appearance of radioactivity in mature</p><p>leaves can be due to the lateral movement of [14C]ABA in the xylem due to transpiration flow</p><p>(Abo-Hamed et al., 1981).</p><p>Cacao seedlings under optimal irrigation conditions also show flush growth, which is</p><p>related with changes in the flush ABA levels (Orchard et al., 1980). These observations</p><p>suggest that, despite adequate water supply, the seedlings suffer from an internal water deficit</p><p>when the water uptake rate by the root system is lower than the rate of losses by leaf</p><p>transpiration. This would cause the accumulation of ABA in the apex and, consequently, the</p><p>imposition of apical bud inactivity at least in part of the interflush period. This hypothesis</p><p>was confirmed by Abo-Hamed et al. (1983) after relating physical parameters (leaf blade</p><p>position, population of hairs, cuticle thickness and number of stomata) of leaves of a new</p><p>flush with transpiration and, therefore, with the water balance of cocoa seedlings in different</p><p>stages of the flush cycle.</p><p>The decrease in diffusive resistance and increase of water loss at the I-1 stage coincide</p><p>with the period of higher ABA levels in leaves of the new as well as previous older</p><p>flushes</p><p>(Orchard et al., 1980). This formation of ABA after stage F-2 could be the result of water</p><p>stress created by leaf transpiration exceeding the capacity of water uptake. The rate of</p><p>maximum water loss of a new flush is only reached when the leaves are fully expanded,</p><p>stomata completely developed and the leaves horizontally positioned (Abo-Hamed et al.,</p><p>1983).</p><p>Cacao: Ecophysiology of Growth and Production</p><p>49</p><p>Iserentant (1976), comparing the effects of removal of all leaves of cacao seedlings in</p><p>stages equivalent to F-1 and I-2 of the flushing cycle, verified the break of apical dormancy</p><p>after defoliation in both stages. Iserentant (1976) concluded that quiescence in seedlings was</p><p>due to correlative inhibition instead of a true dormancy. Similar results were found by Abo-</p><p>Hamed et al. (1981) when only leaves in stages F-2 and I-2 of a new flush were removed.</p><p>This suggests that there are no reversible or irreversible stages in cacao seedlings (Abo-</p><p>Hamed et al., 1981), as described by Vogel (1975) for cacao trees grown under field</p><p>conditions. However, even in plantlets, it seems that two physiological stages exist in the</p><p>period of bud growth inhibition (Abo-Hamed et al., 1981).</p><p>Nutrient X ABA Interactions</p><p>Vogel (1975) described the initial phase of quiescence as a reversible phase that occurs</p><p>during F-2 (Abo-Hamed et al., 1981). It appears that this phase in cacao seedlings can be</p><p>initiated by the competition for nutrients between the apex and the developing leaves of the</p><p>flush. According to Orchard et al. (1980), F-2 leaves of a new flush contain low levels of</p><p>ABA and, consequently, are not the source of this compound. Since the removal of leaves in</p><p>the flush stimulates the apical bud to produce new leaves, this stimulus could result in the</p><p>removal of a powerful drain for nutrients instead of the removal of an ABA source (Abo-</p><p>Hamed et al., 1981). Only the second phase, previously known as the irreversible phase</p><p>(dormancy in I-1 and I-2), is controlled by the transport of ABA from mature leaves to the</p><p>apex. In this case, the role of ABA seems to be in maintaining rather than initiating apical bud</p><p>quiescence (Abo-Hamed et al., 1981).</p><p>Removal of new flush leaves at the I-2 stage causes reduction in the quiescence period of</p><p>the apex (Abo-Hamed et al., 1981). Since in this period the new flush leaves contain high</p><p>ABA levels (Orchard et al., 1980), probably the inhibitory effect of new flush leaves in I-2 is</p><p>due to ABA and its transport to the apex (Abo-Hamed et al., 1981). The removal of previous</p><p>flush leaves at the I-1 stage also promotes reduction in the apex dormancy period. These</p><p>mature leaves are sinks for nutrients (Abo-Hamed et al., 1981) and also contain high ABA</p><p>levels (Orchard et al., 1980) and, therefore, they could serve as an ABA source for the apex,</p><p>like mature leaves of new flushes (Abo-Hamed et al., 1981).</p><p>Application of ABA always extends the inactive period of growth. Alternatively, the</p><p>application of growth promoters (GA3 or zeatin) reduces the duration of the subsequent</p><p>quiescence stage of the apex. Probably, endogenous inhibitors in leaves are overcome by the</p><p>effects of growth promoters that shorten the quiescence period. On the other hand, the fact</p><p>that GA3 applied to new flush leaves in the F-2 stage does not promote a reduction effect on</p><p>the duration of the apex dormancy period reinforces the hypothesis that the apical dominance,</p><p>at this stage, is due to competition by nutrients instead of the presence of hormonal inhibitors</p><p>in the leaves (Abo-Hamed et al., 1981).</p><p>Source–Sink Relationships</p><p>Developing leaves display a low photosynthetic capacity (Baker and Hardwick, 1973)</p><p>and are considered sinks for photoassimilates during most of the expansion phase. During this</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>50</p><p>period, leaf contents of fructose, glucose and sucrose increase, presumably due to imports</p><p>from older leaves. However, when leaf expansion ends, glucose and fructose pools decline</p><p>and sucrose concentration increases, which reflects the end of photoassimilate import and the</p><p>beginning of endogenous sucrose synthesis (Baker and Hardwick, 1975). The simultaneous</p><p>development of several leaves within a flush constitutes, however, a very large carbohydrate</p><p>consumption event during a period of 10 to 15 d that exceeds the available current</p><p>photosynthate (Machado and Hardwick, 1988b). Although there is little competitive influence</p><p>among developing leaves within the flush, leaves that develop at the end of a normal flush,</p><p>are smaller in size (Machado and Hardwick, 1988a). This strongly suggests that the</p><p>subsequent leaves in a normal flush grow under the increasing deficit of a presumable factor</p><p>that supports growth, such as carbohydrate, which may negatively influence the potential for</p><p>full size growth. In the interflush the stock of carbohydrates is reestablished, and, with the</p><p>return of a favorable carbohydrate balance, the appearance of a new flush can occur</p><p>(Machado and Hardwick, 1988b).</p><p>F-2 leaves of a new flush also represent a powerful sink for nutrients, which would be in</p><p>competition with the shoot meristem (Abo-Hamed et al., 1981). Chemical composition of</p><p>cacao leaves showed significant decrease in total N levels of mature leaves during the</p><p>development of a new flush (Santana and Igue, 1979). This decline was attributed to an</p><p>increase in N mobilization from mature to expanding leaves. At this stage in the flushing</p><p>cycle, there is a large quantity of endogenous auxin (Orchard et al., 1981) and a high rate of</p><p>14C translocated out of the labeled leaf as compared with other stages (Sleigh, 1981).</p><p>Additionally, at the beginning of F-2, the amount of carbohydrate translocated from mature</p><p>leaves to the developing flush exceeds (positive balance) that required for leaf growth. This</p><p>excess can be stored in the newly formed stem and used for its expansion, mainly in mid F-2,</p><p>when the leaves of the flush constitute a very strong carbohydrate drain, and the amount</p><p>required for leaf growth considerably increases (Machado and Hardwick, 1988b).</p><p>In the I-2 stage, new flush leaves are completely expanded, show maximum</p><p>photosynthetic capacity, and are capable of photoassimilate export (Baker and Hardwick,</p><p>1975). At the end of this stage, cytokinin, imported from the root, accumulates in the apical</p><p>bud and helps to activate the breaking of bud quiescence in the transition to stage F-1 (Alvim</p><p>et al., 1974b; Orchard et al., 1981). Observations reported by Sleigh (1981) and later</p><p>confirmed by Machado (1986) showed that, at the F-2 stage, expanding leaves import</p><p>considerable amounts of 14C that is assimilated by the mature leaves. Unexpectedly, if a high</p><p>proportion of photoassimilates is removed from mature leaves during the F-2 stage, a</p><p>corresponding increase of photosynthesis does not occur. This suggests that the requirement</p><p>of carbon for growth, at least for leaves, does not directly control photosynthesis of mature</p><p>cacao leaves (Machado and Hardwick, 1988b). According to Baker and Hardwick (1973), A</p><p>of older leaves, with 90% more Chl, is only 10-20% higher than that of leaves at the end of</p><p>flushing. Consequently, the photosynthetic efficiency of older leaves is significantly smaller.</p><p>Therefore, in leaves of cacao, the decline in photosynthetic efficiency occurs during the</p><p>period between the end of flushing and onset of senescence.</p><p>Cacao: Ecophysiology of Growth and Production</p><p>51</p><p>Climate</p><p>Information exists about the periodicity of cacao leaf production in relation to changes of</p><p>climatic elements, especially the effect of temperature (Couprie, 1972), solar radiation</p><p>(Snoeck, 1979), and rainfall (Alvim and Alvim, 1978). Almeida et al. (1987), carried out a</p><p>study in Ilhéus, Bahia state, Brazil, that investigated the relationship between actual</p><p>evapotranspiration and reference evapotranspiration to quantify the effects of water deficit on</p><p>cacao</p><p>flushing. The actual-to-reference evapotranspiration ratio was used in the original</p><p>expression of degree-day in order to evaluate the concomitant effects of temperature and</p><p>water on flushing. Nominating this weighted function penalized degree-days (PDD), Almeida</p><p>and co-workers verified that the weighted function represented approximately 80% of the</p><p>existing interactions between flushing and weather factors. The high degree of significance of</p><p>this function is due to the fact that PDD represents the joint effects of energy and water. For</p><p>the conditions of Bahia the PDD that best explained flushing was that calculated three weeks</p><p>before leaf emission. In Bahia, the main flushing period, characterized by relatively short</p><p>periods of vegetative rest, is from September to February. During those months, the energy</p><p>curve (averages day-1) is in ascension and coincides with the period of more intense flushing</p><p>(Almeida et al., 1987). Furthermore, in that area, the mean air temperature at the 8th week,</p><p>combined with the solar radiation and insolation of the 9th week, exert great influence on</p><p>flushing. In contrast, the period of decreasing energy (solar radiation, temperature and PDD)</p><p>coincides with those months in which no flushing occurs (Almeida et al., 1987).</p><p>The seasonal influence of temperature on phenological events is evident in the flowering,</p><p>fruiting and pod growth profiles found by Cazorla et al. (1989), who also observed low</p><p>flushing during June to September. This period is characterized by relatively low</p><p>temperatures. Therefore, the absence of flushing and flowering in south Bahia is intimately</p><p>related to the decrease of fruiting, which culminates with an almost total absence of pods</p><p>from January to March of the following year (Leite and Valle, 2000). In Bahia, cacao usually</p><p>stops flushing from March to July and remains in a relative vegetative rest afterwards (Alvim,</p><p>1977). Therefore, the period of minimum flushing varies from 90 to 120 d – June to</p><p>September (Alvim et al., 1974a).</p><p>Alvim et al. (1974a), Alvim (1977) and Almeida et al. (1987) studied the influence of</p><p>rainfall and water balance on flushing within defined months of the year. According to Alvim</p><p>(1977), in most cacao producing areas, the beginning of leaf emission follows the first rains</p><p>after a dry period. According to Sale (1968), rainfall or irrigation, after a dry period, is a</p><p>necessary condition to elicit flushing. However, under field conditions, flushing begins in</p><p>response to an increase of plant Ψw, but not necessarily to rainfall, after a period of humidity</p><p>stress (Almeida et al., 1987). Once apical bud growth resumes, rainfall plays a decisive role</p><p>on leaf expansion. This may be one of the possible reasons to best explain the vigorous</p><p>flushing associated with rainfall that follows a period of humidity stress (Alvim, 1977).</p><p>Almeida et al. (1987) showed that during the vegetative inactive period, the changes in</p><p>soil moisture availability and, consequently, the sequence of water deficits and excesses, do</p><p>not seem to play a direct role in the phenomenon of bud dormancy break. However, once the</p><p>apical bud dormancy is broken, water availability seems to exert great influence on the</p><p>intensity of leaf emission. Therefore, flushing becomes relatively intense when the period of</p><p>water deficit (storage of water in the soil below 50 mm) is followed by rains that replenish</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>52</p><p>soil water content (Almeida et al., 1987). Similar results were found by Sale (1968), Alvim</p><p>(1977) and Machado and Alvim (1981).</p><p>Physiological responses of cacao are affected when the soil water content is below 60-</p><p>70% of the maximum available soil water capacity (Alvim, 1960). Therefore, the</p><p>development of water deficit during the dry season is considered an important factor in the</p><p>control of flushing in field-grown cacao plants (Alvim et al., 1974a). At the beginning of a</p><p>new flush cycle the transition from inactivity to apical growth of a branch occurs immediately</p><p>following the decrease of water deficit. This is exhibited through leaf shedding at the</p><p>beginning of the rainy season and the consequent reduction of the high shoot ABA levels in</p><p>the preceding period of water deficit (Alvim et al., 1974b). In contrast, the effects on the</p><p>apical bud activity, triggered by dry periods followed by rain, seem to occur through</p><p>modifications of the ABA:cytokinin balance. Increase in the ABA:cytokynin ratio inhibits</p><p>flushing (Alvim et al., 1974b). Removal of mature leaves produces modifications in that</p><p>balance as well. Therefore, after defoliation, ABA content in the apical bud decreases, while</p><p>cytokinins content increases considerably (Alvim and Alvim, 1976).</p><p>In tropical climates temperature oscillations are relatively small compared to temperate</p><p>climates. Nonetheless, trees grow intermittently within seasonal climatic sequences, and</p><p>flushing is considered the beginning of a growth cycle (Alvim, 1977). For cacao grown in</p><p>southeastern Bahia, the flowering, fruiting and pod growth patterns show low flushing in June</p><p>to September (Cazorla et al., 1989), a period characterized by relatively lower temperatures</p><p>(Leite and Valle, 2000). According to Almeida et al. (1987), temperatures above a reference</p><p>value (around 23°C) coincide with periods of increased flushing. Similar responses were</p><p>observed under controlled conditions by Sale (1968), when cacao plants submitted to 23.3,</p><p>26.6 and 30°C emitted leaves respectively at 95, 36 and 20 d intervals. Therefore, it seems</p><p>that high temperatures accelerate flushing initiation.</p><p>Role of Endogenous Factors on Cacao Flowering</p><p>Cacao produces caulescent flowers that arise from meristematic tissues above leaf scars</p><p>on the woody stems that are at least 2-yr-old (Figure 4). The floral meristem or cushion</p><p>produces flowers throughout the life span of the tree (Aneja et al., 1999). Cacao flowers</p><p>contain different polyphenolic compounds such as: (i) hydroxycinnamic acids, found in in the</p><p>periphery of the organs, except in the ovary where parenchyma cells are present and the</p><p>ovules occur; (ii) tannins; and (iii) anthocyanins. Both tannins and anthocyanins are located in</p><p>the epidermis of different floral parts. Anthocyanins are mainly restricted to ornamentation in</p><p>petals and staminoids (Alemanno et al., 2003). These external locations of phenolic</p><p>compounds may function as chemical protective barriers against damages caused by pests and</p><p>diseases (Alemanno et al., 2003).</p><p>In each flower the sepals begin to dehisce in late afternoon, and the flower is completely</p><p>open at the beginning of the following morning. During this period the anthers liberate pollen</p><p>and the stigma is receptive (Aneja et al., 1999). Although cacao flowers are hermaphroditic,</p><p>the anthers are covered by the lower half of the petals. Without the intervention of insects,</p><p>mainly Forcipomyia sp. (Diptera: Ceratopogonidae), pollination is impaired, since the viscous</p><p>pollen does not come into contact spontaneously with the stigma (Dias et al., 1997). In Bahia,</p><p>Cacao: Ecophysiology of Growth and Production</p><p>53</p><p>Brazil, high populations of this insect are found from March to July, which coincides with the</p><p>increased pollination that results in the main harvest.</p><p>Figure 4. Counterclockwise: flowering on the trunk and branches of an adult tree, flowering in a 9-</p><p>month-old seedling in the field and details of a flower cushion. Photos by the authors.</p><p>The fly populations are low during the high temperature months. This is reflected in the</p><p>low and sporadic productivity that follows this fruit setting period (K. Nakayama, 2007;</p><p>unpublished results). If the flowers are not pollinated, they abscise 24-36 h after anthesis,</p><p>without visible signals of senescence (Aneja et al., 1999; Hasenstein and Zavada, 2001). If</p><p>pollination is accomplished and fertilization occurs, the ovary increases in size, the pedicel</p><p>enlarges, and the corolla wilts and</p><p>deteriorates (Aneja et al., 1999).</p><p>The genus Theobroma represents an atypical example of an ovarian auto-incompatibility</p><p>system that is distinct from most vegetal incompatibility systems (de Nettancourt, 1977).</p><p>Incompatibility in cacao was first reported by Pound (1932), who noted the occurrence of</p><p>changes from self-incompatibility to self-compatibility during certain periods of the year. The</p><p>incompatibility system in cacao is complex, since it includes different degrees of cross and</p><p>self-incompatibility of some genotypes as well as a high level of self-pollination (Lanaud et</p><p>al., 1987).</p><p>Although there is no causal link between expression of enzymatic activity and</p><p>incompatibility, Warren and Sunnite (1995) argued that enzymes like isocitrate</p><p>dehydrogenase, malate dehydrogenase and acid phosphatase are indicative of incompatibility</p><p>systems. In contrast, Aneja et al. (1992, 1994) showed that the pollen grains of the self-</p><p>incompatible clone ‘IMC-30’ did not germinate at low CO2 partial pressure. However, ‘IMC-</p><p>30’ pollen grains germinated under high CO2 concentration, which helped overcoming</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>54</p><p>incompatibility in self-pollinated flowers. The main effect of overcoming incompatibility</p><p>systems in self-incompatible genotypes occurs when self-incompatible and compatible</p><p>(foreign) pollen are mixed, which permits self-fertilization in self-incompatible trees</p><p>(Glendinning, 1960; Bartley, 1969; Lanaud et al. 1987). These results imply that, in</p><p>Theobroma, a substance other than CO2 may condition the maternal plant self-fertilization</p><p>(Hasenstein and Zavada, 2001).</p><p>The percentage of flowers that sets pods in cacao is usually very low and varies from 0.5</p><p>to 5% (Aneja et al., 1999). This is partly due to the fact that the effective rate of self-</p><p>fertilization in auto-incompatible trees is low, whereas in self-compatible trees self-</p><p>fertilization can reach up to 43% (Yamada and Guries, 1998). The success of fruit (pod) set</p><p>can depend on two factors, the degree of pollen compatibility and the number of pollen grains</p><p>deposited on the stigma (Lanaud et al., 1987). There is some evidence that a high number of</p><p>pollen grains is beneficial for overall pod set (Hasenstein and Zavada, 2001). Moreover, a</p><p>high proportion of pollinations results from the visit of a single pollinator (Yamada and</p><p>Guries, 1998). At anthesis floral auxin concentration is low and the retention of flowers, as</p><p>well as fertilization and possibly pod development, depend on an external source or signal for</p><p>satisfactory pollen germination or fertilization, as found by Hasenstein and Zavada (2001).</p><p>They also noted an inverse correlation between the number of flowers per plant and floral</p><p>auxin content and suggested that the genetic control of self-incompatibility in cacao may be</p><p>modulated by the hormonal content of the flower. Hasenstien and Zavada (2001) concluded</p><p>that this variation in floral hormonal content could explain the great number of pods set in</p><p>some instances, even after incompatible pollinations.</p><p>A better understanding of the factors involved in floral abscission can be of great</p><p>horticultural value (Aneja et al., 1999). Abscission of flowers in cacao occurs within 2-3 d</p><p>after anthesis in the absence of pollination or fertilization. Even after manual pollination, only</p><p>a small percentage of pollinated flowers develops and produces pods (Hasenstein and Zavada,</p><p>2001). Although there is no recognizable abscission area in the flower pedicel at anthesis,</p><p>within 24 h starch grains appear in the pedicel cortex in the area of the incipient abscission</p><p>zone, and cell separation occurs in the epidermis at 2-3 mm acropetally from the point of</p><p>pedicel attachment to the flower pad (Aneja et al., 1999). Flower abscission due to</p><p>incompatible pollination begins before the pollinic tube reaches the ovules (Aneja et al.,</p><p>1994; Baker et al., 1997).</p><p>It has been observed that auxin concentration of developing floral buds is high and</p><p>depends on the number of flowers formed. However, when the buds mature, the auxin level</p><p>decreases during the initiation of the abscission process (Hasenstein and Zavada, 2001), while</p><p>ABA levels of the flower increase significantly before abscission (Aneja et al., 1999). In</p><p>contrast, most of the increase in ethylene production occurs simultaneously with abscission</p><p>(Aneja et al., 1999). There is no abscission in the absence of ABA even when ethylene is</p><p>present. Therefore, in cacao flowers, ABA seems to be the primary inductor of abscission,</p><p>while ethylene, although accelerating abscission does not seem to be required for the process</p><p>(Aneja et al., 1999). The increase of indoleacetic acid (IAA) levels in the cacao ovary, that</p><p>follows compatible pollination and fertilization (Baker et al., 1997), or application of</p><p>naphthalene acetic acid, can overcome the effect of ABA in the formation of the abscission</p><p>area and reduce floral senescence (Aneja et al., 1999).</p><p>Hormonal changes after compatible and incompatible pollination indicates a strong</p><p>increase of endogenous auxin after compatible pollination and a strong increase of ethylene</p><p>Cacao: Ecophysiology of Growth and Production</p><p>55</p><p>after incompatible pollination (Baker et al., 1997). These hormonal responses occur before</p><p>the interaction of the pollin tube with the ovule and suggest that the incompatibility system</p><p>may be influenced by auxin (Hasenstein and Zavada, 2001). According to Aneja et al. (1994),</p><p>the ability of CO2 to overcome abscission and the subsequent self-compatibility can be the</p><p>result of minimization of ethylene effects. However, it is conceivable that high auxin levels</p><p>also override the abscission signal, affecting or controlling the auto-incompatibility response</p><p>in Theobroma (Hasenstein and Zavada, 2001).</p><p>Since flower production represents a considerable plant investment (Valle et al., 1990),</p><p>the number of flowers can affect the auxin partition to each flower. This may explain the low</p><p>concentration of endogenous auxin in clones with high flower productions (Hasenstein and</p><p>Zavada, (2001). Auxin concentration is significantly higher in cacao clones with low</p><p>production of flowers. Producers of a high number of flowers can show a 20-fold</p><p>improvement in pod set, in spite of the existence of a poor relationship between pod and</p><p>flower number. In addition, there is a strong negative correlation between the number of</p><p>flowers produced and the endogenous content of IAA, while the content of ABA did not</p><p>differ between the two sets (Hasenstein and Zavada, 2001).</p><p>EFFECTS OF ABIOTIC FACTORS ON YIELD</p><p>The adult stage of cacao is reached when the tree enters reproductive growth. Pod</p><p>production is small during the first years and increases as the tree matures. In general, most of</p><p>the pod yield is found on the trunk and branches (Figure 5). Bartley (1970), studying the yield</p><p>of cacao per tree, proposed to initiate selection of potentially high-yielding cacao trees in the</p><p>8th yr of planting. Since with young trees fruit bearing begins approximately at the 4th yr, it</p><p>has been suggested that only at the 8th or 10th year after planting do the trees express their</p><p>productivity potential (Dias and Kageyama, 1997).</p><p>Also, measurements of diameter and stem height, average crown diameter and leaf area</p><p>of cacao trees between 1- to 3-yr-old have been used as variables to estimate the yield</p><p>capacity of cacao (Batista and Alvim, 1981; Garcia and Nicolella, 1985). However, the same</p><p>abiotic stresses that reduce pod production can also indirectly decrease yield by increasing the</p><p>duration of the juvenile period, which varies widely within cacao genotypes. Flowering, for</p><p>instance, in some cacao hybrids can begin 18 months after planting in the field, while in other</p><p>genotypes flowering may be initiated after 3 to 5 yr (Sena Gomes and Kozlowski, 1986).</p><p>The most important determining biotic parameters of cacao yield are related to (i) light</p><p>interception, photosynthesis</p><p>and capacity of distributing photoassimilate, (ii) maintenance</p><p>respiration, and (iii) pod morphology and seed formation (Zuidema et al., 2005). These three</p><p>items are crucial to seed yield and were examined in initial studies concerning cacao</p><p>production (Yapp and Hadley, 1994). On the other hand, these biotic parameters can be</p><p>modified by abiotic factors, such as those inhibiting, for instance, initiation of floral buds</p><p>(Alvim, 1977) or those that, after flowering and pod set, influence pod development (Wood,</p><p>1985). Climatic changes exert outstanding effects in the flush cycle, an important determinant</p><p>factor of yield (Almeida et al., 1987).</p><p>In the definition of an appropriate climate for cacao cultivation in forest understorey</p><p>conditions, it is well known that their microclimatic variables are completely different from</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>56</p><p>the standard weather conditions outside that environment (Bonaparte and Ampofo, 1977).</p><p>Also, there are indications that the structure and dynamics of the cacao agroecosystem exert</p><p>some influence in the microclimate (Beer, 1987). Air temperature, RH and rainfall are</p><p>correlated and affect the seasonality of microclimatic conditions inside a cacao plantation</p><p>(Miranda et al., 1994). The magnitude of the meteorological parameters varies less in a hot</p><p>week than in a cooler week. The predominantly clear summer (average of 9 h daily sunshine)</p><p>and the cloudy winter (average of 5 h daily sunshine) regulate, to a great extent, the behavior</p><p>of microclimatic parameters above and inside a cacao plantation.</p><p>Figure 5. Most cacao pods are beared in the trunk. Cacao pods of two different genotypes. Photos by</p><p>the authors.</p><p>Temperature</p><p>According to Daymond and Hadley (2004), temperature is one of the main limiting</p><p>factors for cacao production, since temperature stress affects the seasonal variation in seed</p><p>yield. In a cacao plantation, the difference in temperature measured outside and inside canopy</p><p>layers was around 2 ± 0.5°C, although higher values have been registered during summer</p><p>weeks. The undercanopy maximum temperatures are characterized by drops varying from 1</p><p>to 3°C and temperature differences inside the canopy vary from 2.5 to 4°C, while the above</p><p>canopy maximum temperature decreased from 1.5 to 3.5°C (Miranda et al., 1994). When</p><p>measuring leaf temperature in the upper canopy layer of a non-shaded cacao tree on a sunny</p><p>day, Valle et al. (1987) verified that it was always 2°C above the leaf temperatures of the</p><p>middle and lower canopy layers. Leaves of the upper canopy layer showed higher differences</p><p>between leaf and air temperature and, therefore, water vapor deficit, in comparison to lower</p><p>layers.</p><p>Water and Light</p><p>Several factors influence leaf dynamics, among them water and light availability, which</p><p>largely vary between locations and cropping systems (Zuidema et al., 2005). Additionally,</p><p>Cacao: Ecophysiology of Growth and Production</p><p>57</p><p>wind conditions during the dry season reduce cacao yield due to water loss and reduction of</p><p>leaf area (Alvim, 1977; Leite et al., 1980). Southeastern Bahia is a region with an average</p><p>annual temperature of 23.5°C, annual total rainfall of approximately 1700 mm, no</p><p>pronounced dry season, and trees are shaded with E. fusca and/or E. poeppigiana. Here the</p><p>relative light intensity received by cacao trees cultivated varies between 30 and 100% of full</p><p>sunlight and 4 to 10% radiation at soil level. The average leaf area index and the extinction</p><p>coefficient are about 3.9 and 0.61, respectively (Miyaji et al., 1997a). Leaf longevity varies</p><p>with position inside the canopy and/or incident irradiance, time of emergence and height in</p><p>relation to the soil level. According to Miyaji et al. (1997b) for Catongo trees of about 7-yr-</p><p>old the leaf duration at heights greater than 220 cm and above 60% full sunlight is 181 d,</p><p>which is half the duration of leaves at heights between 0-150 cm and 5 to 20% sunlight.</p><p>Factors like soil water deficit and leaf respiration, due to high air temperature and high</p><p>radiation can be causes for the intensive leaf fall in the middle and upper canopy layers of the</p><p>cacao crown (Alvim and Alvim, 1978).</p><p>The cacao yield is strongly related to rainfall in the dry season. It also depends on soil</p><p>type and consequently water retention capacity (Zuidema et al., 2005). According to Leite and</p><p>Cadima Zevallos (1991), the elevation and residence of the water table lead to increase and</p><p>maintenance of humidity levels above the subsurface of the soil, a zone in which the cacao</p><p>root system concentrates in traditional cacao cropping areas. To reach high levels of cacao</p><p>yield in south Bahia, the monthly rainfall totals should be equal or greater than 200 mm,</p><p>while the permanence of the water table should be more than 30 d (Leite and Valle, 2000).</p><p>The fluctuation of the water table can be considered a climatic variable (derived from rainfall)</p><p>that can influence cacao production as a form of natural sub-irrigation (Leite and Valle,</p><p>2000).</p><p>Using a simulation model, Zuidema et al (2005) showed that annual solar radiation and</p><p>rainfall during the dry season explained 70% of the variations in annual seed yields obtained</p><p>for 30 sites along the tropical cacao producing areas of the world. Drought promotes</p><p>decreases in leaf area (Orchard and Saltos, 1988), A (Hutcheon, 1977), flowering (Sale, 1970)</p><p>and yield (Khan et al., 1988). Changes in carbon distribution and export will depend on the</p><p>severity and duration of the stress, as well as its occurrence in relation to flowering, pod set</p><p>and pod maturation (Deng et al., 1989). There are positive correlations between yield and</p><p>rainfall during months that precede harvest (Alvim, 1978), where rain distribution is more</p><p>important than its magnitude (Atanda, 1972). Alvim (1988) considered that harvest can be</p><p>influenced by the rain distribution that occurred six months prior. This relationship seems</p><p>valid for countries such as Brazil (southeastern Bahia), Ghana, Ivory Costa and Malaysia. In</p><p>Bahia, the agricultural cacao calendar year begins in April and extends to March. The yield is</p><p>divided into two distinct periods, minor harvest (temporão) from April to August and main</p><p>harvest (safra) from September to March. The relative importance of each harvest depends on</p><p>rain distribution (Alvim, 1973). Furthermore, cacao pods take approximately from six to</p><p>seven months to complete their development (Almeida and Valle, 1995). This explains the</p><p>importance of higher rainfall and longer phreatic residence of the water table at the soil</p><p>subsurface in one year for high production in the following year (Leite and Valle, 1990; Dias</p><p>and Kageyama, 1997).</p><p>According to Valle et al. (1987), data modeled for transpiration showed that, on a cloudy</p><p>day, a non-shaded cacao tree could transpire about 45 L (1.2 L m-2 d-1). This assumes that all</p><p>leaves are transpiring at the same rate. A shaded cacao tree, in contrast, could transpire about</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>58</p><p>26 L (0.8 L m-2 d-1). However, on a sunny day both trees showed a substantial difference in</p><p>transpiration when compared with a cloudy day. The daily E was estimated to be 90 L tree-1</p><p>(2.4 L m-2 d-1) for the unshaded tree and 40 L tree-1 (1.2 L m-2 d-1) for the shaded one when</p><p>100% of its leaf area was exposed to incident irradiance (Valle et al., 1987). Estimates of</p><p>daily E on a cloudy day for both tree conditions and for the shaded canopy layers on a sunny</p><p>day were of the same order of magnitude of those calculated by Cadima and Alvim (1983).</p><p>However, for unshaded trees, on a sunny day, Valle et al. (1987) showed an average E more</p><p>than twice the estimated by Cadima and Alvim (1983). From the estimations of LAI (Miyaji</p><p>et al., 1997a) and radiation (Valle et al., 1987), it is concluded that more than 60% of the</p><p>water can be transpired by the upper canopy layers of unshaded cacao trees. In the shaded</p><p>trees less than 5% of the absorbed water might be transpired by the upper layers, which is</p><p>caused by the greater irradiance received in the lower layers than in the top layers due to the</p><p>shade tree that limits light penetration to the upper layer even at lower solar angles.</p><p>Shade vs Unshaded Cropping</p><p>In its natural habitat wild cacao grows under shade trees, but with a low pod production</p><p>(Murray and Nichols, 1966), since the shade trees compete with cacao for water, nutrients and</p><p>light (Bonaparte, 1975). In fact, many people believe that shade is indispensable for cacao</p><p>cultivation (Owusu, 1978) and, therefore, earlier cacao plantations were conducted under</p><p>shade regardless of yield (Urquhart, 1961).</p><p>Evans and Murray (1953) in Trinidad, Alvim (1959) in Costa Rica and Cunningham and</p><p>Lamb (1959) in Ghana were the pioneers to critically examine the role of shade and light in</p><p>cacao cultivation. In a shade and manurial experiment in Ghana strong reductions in yield</p><p>were observed due to shading (Ahenkorah et al., 1974). In fact, cacao grown at full sunlight</p><p>produced more pods than when grown under shade (Owusu, 1978). Control of both growth</p><p>and density of cacao trees, and the increase in aeration and light penetration throughout the</p><p>canopy are fundamental cultural practices necessary to promote increased seed production</p><p>(Vernon and Sunderam, 1972). More recently the comprehensive work of Ahenkorah et al.</p><p>(1987) further elucidates the importance of appropriate fertilization in unshaded cacao</p><p>plantations.</p><p>Studies on light interception and photosynthesis show that seed production is light</p><p>limited, probably due to external and internal shade (self-shading) in the cacao stand and light</p><p>extinction inside the canopy (Yapp and Hadley, 1994). In fact, light intensities below 1800 h</p><p>yr-1 suppress flower production with a significant negative effect on pod yield (Asomaning et</p><p>al., 1971). Heavy shade not only reduces seed yield (Zuidema et al., 2005), because of low</p><p>photosynthate production (Alvim, 1977; Ng, 1982), but also increases the incidence of</p><p>diseases (Alvim, 1977). On the other hand, cacao is a shade tolerant species (Guers, 1985), in</p><p>which appropriate shading could lead to adequate photosynthetic rates, growth and seed yield.</p><p>Shading also alleviates effects of unfavorable ecological factors, such as wind velocity and</p><p>excessive evapotranspiration (Miyaji et al., 1997a; Beer et al., 1998) and, consequently,</p><p>decreases in both humidity stresses and extreme air and soil temperatures during the dry</p><p>season are to be expected (Anim-Kwapong, 2003). This is essential for survival and</p><p>establishment of cacao seedlings in dry and seasonally humid environments (Beer, 1987),</p><p>since the seedlings are highly susceptible to dry periods (or soil moisture stress) (Leite et al.,</p><p>Cacao: Ecophysiology of Growth and Production</p><p>59</p><p>1980). Furthermore, shelter trees used for shade greatly contribute to the formation of soil</p><p>organic matter, carbon sequestration, nutrient recycling and maintenance of biodiversity</p><p>(Lobão et al., 2007; Müller and Gama Rodrigues, 2007). Specifically in regions with low</p><p>access to inorganic fertilizers, the multistrata plantation is used to maintain soil fertility with</p><p>the subsequent increase in nutrient availability for cacao (Isaac et al., 2007).</p><p>When nutrient availability is not a growth-limiting factor, there is a positive correlation</p><p>between cacao yields and light (Bonaparte, 1975; Ahenkorah et al., 1987). Vernon (1967)</p><p>concluded that the relationship between cacao yield and available light was approximately</p><p>linear from 30 to 60% full sunlight. However, when modeled from 0 to 100%, a quadratic</p><p>model showed better adjustment than the simple linear model, suggesting that some degree of</p><p>shading is desirable.</p><p>The higher production of non-shaded cacao results in a shorter productive lifespan, a</p><p>larger demand for fertilizers (Owusu, 1978), a decrease in the incidence of cherelle wilt</p><p>(Asomaning et al., 1971) and larger investments (Ahenkorah et al., 1987). The subsequent</p><p>decline in productivity (Bonaparte, 1973) is attributed to high losses of exchangeable bases in</p><p>the soil, attack of insects and diseases, excessive leaf transpiration and increase in soil</p><p>evaporation (Ahenkorah et al., 1974). The inherent high risk of unshaded cacao cultivation</p><p>was illustrated by the economic analyses of Cunningham (1963), the extra expenditure and</p><p>work associated with clear-felling and growing unshaded cacao with great amounts of</p><p>fertilizers would probably be justifiable only if yields of more than three tons are obtained.</p><p>However, most of the cacao experiments involving shade and fertilizers show that shade</p><p>reduces the responses to fertilizer applications (Alvim, 1977), and such conditions are rarely</p><p>economically justifiable (Beer, 1987). This shows that cacao production is positively related</p><p>to light intensity (Vernon, 1967), but this relationship depends primarily on the availability of</p><p>nutrients in the soil (Figure 6).</p><p>Figure 6. Cacao grown under different shade and fertilizer regimens in Ghana. From Ahenkorah et al.</p><p>(1974) with permission of the American Society for Horticultural Science.</p><p>Alex-Alan F. de Almeida and Raúl R. Valle</p><p>60</p><p>In commercial plantations it is hard to understand and detail the potential productivity in</p><p>relation to pod-set and yield, since the cacao canopies are under several shade levels (Alvim,</p><p>1977). With shade management practices cacao production can increase during the first</p><p>decade and thereafter stabilizes (Rosenberg and Marcotte, 2005). Cacao trees can produce</p><p>during 30 to 80 yr (Stevenson, 1987); however, yield subsequently decreases (Rosenberg and</p><p>Marcotte, 2005). Furthermore, it is probable that the physiology of trees under heavy shade</p><p>would be modified, because shaded trees can be more efficient in photosynthesis and leaf</p><p>dynamics (rates of production and abscission), as, for example, the increase in leaf lifespan</p><p>(Miyaji et al., 1997a). According to Owusu (1978), there is a close relationship between these</p><p>physiological processes and carbohydrates in cacao. Improved growth, increase of flushing,</p><p>enhanced flowering and increased yield under unshaded conditions can, however, be</p><p>explained in terms of increase in carbohydrate production (Asomaning et al., 1971). This is</p><p>exemplified by the internal competition between flowers and pods (Alvim, 1954), in spite of</p><p>the small total energy expenditure for flowering (Valle et al., 1990). Furthermore, Alvim</p><p>(1977) considers that besides the competition within pods, the annual variation of pod set is</p><p>also subject to competition with other vegetative events, such as flushing and root and</p><p>cambium growth.</p><p>CONCLUSION</p><p>The expectation for the next 10 yr, without considering India and China, is a consumption</p><p>increase of nearly one millions tons of cacao seeds. The big question is from where would the</p><p>extra demand come? A strong possibility is an increase in productivity in West African</p><p>countries, but this would be at the expense of significant resource inputs and occur over a</p><p>long period. Actually, the chocolate industry foresees difficulties regarding future supplies.</p><p>Today the world faces a new situation with the search for new renewable energy sources. As</p><p>an example, Malaysia has replaced cacao plantations with oil palm, and Indonesia has</p><p>become less and less interested in producing cacao.</p><p>According to the World Cocoa Foundation (www.worldcocoafoundation.org) there is a</p><p>tendency towards an increase in the consumption of chocolate with high cacao content (43%)</p><p>in Europe and USA. Also, there is a world trend in the proliferation of small companies that</p><p>process cacao and make chocolate. Their search for cacao is remarkable. There is also a</p><p>consensus that in countries with a better level of development, such as Brazil, the future will</p><p>be the investment in quality and production of differentiated cacao. Therefore, the</p><p>efforts in</p><p>Bahia to produce fine cacao is in reality a world tendency for other locations with similar</p><p>environments, thus, constituting a great opportunity for expansion in this market.</p><p>Furthermore, the markets under greatest expansion are those of the emerging nations.</p><p>Therefore, expectations are strong for the inclusion of China and India in the chocolate</p><p>consumption market. However, if the markets show a promising tendency, more and more of</p><p>the cacao farmers will feel the burden of high costs of resource inputs, mainly for control of</p><p>diseases and insects that are steadily increasing. Several pests and diseases attack cacao, with</p><p>some estimates putting losses as high as 30 to 40% of global production</p><p>(www.icco.org/about/pest.aspx). In this sense farmers seek new lands that offer an escape</p><p>from known diseases, and in this respect we may highlight the importance of studying the</p><p>Cacao: Ecophysiology of Growth and Production</p><p>61</p><p>behavior of the crop under semi-arid conditions as mentioned earlier. The knowledge of the</p><p>effects of factors that affect the cacao growth and development under such conditions should</p><p>even make it possible to engineer new practices for the traditional cropping areas.</p><p>ACKNOWLEDGMENTS</p><p>The first author gratefully acknowledges the Conselho Nacional de Desenvolvimento</p><p>Científico e Tecnológico (CNPq), Brazil, for the concession of a fellowship of scientific</p><p>productivity. Thanks are also in order to Prof. Raimundo S. 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Recomposição florística do Parque zoobotânico do Centro de</p><p>Pesquisas do Cacau. Rev. Theobroma 1984;14:1-25.</p><p>Gama-Rodrigues AC, Valle RR, Rossiello ROP. Crescimento, trocas gasosas e relações</p><p>hídricas de plântulas de cacau em função de diferentes fontes de potássio. Rev. Bras.</p><p>Ciên. Solo 1995;19:387-93.</p><p>Garcia JR. Estudo de alguns índices de crescimento e produtividade para seleção juvenil em</p><p>híbridos de cacau. MSc thesis, IICA, Turrialba; 1973.</p><p>Garcia JR, Nicolella G. Correlação entre algumas medidas dendrométricas, origem genética e</p><p>produção de frutos em cacaueiros. Rev. Theobroma 1985;15:113-24.</p><p>Greathouse DC, Laetsch WM, Phinney BO. The shoot-growth rhythm of a tropical tree,</p><p>Theobroma cacao. Am. J. Bot. 1971;58:281-6.</p><p>Guers J. Potentialités photosynthétiques du cacaoyer (Theobroma cacao L.) en fonction de</p><p>l’eclairement, de la température et du CO2 ambiant. Café Cacao Thé 1985;29:245-54.</p><p>Hadley P, End M, Taylor ST, Pettipher GL. Environmental regulation</p><p>plants and their interactions with surrounding environments, for their entire lifecycle or any</p><p>period of their lifecycle. The plant lifecycle is an important aspect responsible for key</p><p>differences among crops’ growth and developmental strategies. With regard to trees, in spite</p><p>of the fact that their basic physiology is similar to that of annual species, there are some</p><p>facets, such as size and complexity of organization, that make them an exciting area of</p><p>diversity. The concept of a tree is amenable to an array of definitions, which usually involve</p><p>size as well as physiognomy. Here, I have considered what is meant by “tree” in a broad</p><p>sense according to the definition of Hallé et al. (1978) summarized in the Merriam-Webster's</p><p>Collegiate Dictionary (Mish, 1993): "… a woody perennial plant having a single usually</p><p>elongate main stem generally with few or no branches on its lower part; a shrub or herb of</p><p>arborescent form…". Such a definition provides a partial justification for the selection of the</p><p>tropical tree crops examined here, embracing not only trees such as mango and rubber but</p><p>also non-woody species such as banana, coconut and oil palm (Table 1). Furthermore, for a</p><p>few tropical tree crops with greater economic importance in the world trade (e.g., citrus and</p><p>coffee) there has been a relatively large amount of basic research on environmental</p><p>physiology, but much less than for temperate tree crops such as apple and stone fruits. Lack</p><p>of fundamental research may be due partially to the fact that the majority of tropical tree</p><p>crops are cultivated in third-world countries where limited resources are available to</p><p>adequately explore the diversity amongst tropical plant species. This is another reason to</p><p>justify the choice of the crops explored in the present book.</p><p>In the majority of chapters of this volume, photosynthesis is treated as a major process</p><p>affecting crop growth and performance. This is not surprising, taking into account that 90-</p><p>95% of plant dry mass is derived from photosynthetically fixed carbon, although a</p><p>straightforward relationship between photosynthesis and crop yield is not always observed</p><p>(Kruger and Volin, 2006). It is highlighted that highly-productive species such as cassava,</p><p>papaya and banana have high photosynthetic rates, with values that may reach as much as 50</p><p>μmol m-2 s-1 in cassava (El-Sharkawy et al., 1992). In contrast, slow-growing crops, such as</p><p>citrus, cocoa and coffee, which have evolved as understory trees, are traditionally considered</p><p>to have very low photosynthetic rates, seldom above 10 μmol m-2 s-1, even in the field under</p><p>Fábio M. DaMatta</p><p>2</p><p>favorable growth conditions (DaMatta, 2003). This behavior has mostly been associated with</p><p>large, diffusive, rather than biochemical, limitations to photosynthesis (DaMatta et al., 2001),</p><p>which can become increasingly important, particularly under stressful conditions such as</p><p>drought and elevated temperatures.</p><p>Table 1. Brief description of the tropical tree crops dealt with in this book. Unless</p><p>otherwise stated, for all species, fruits are the harvestable yield. Sources: Alvim and</p><p>Koslowski (1977), León (1987), Smith et al. (1992), and Last (2001)</p><p>Scientific name Common name Probable origin/Areas of cultivation/Remarks</p><p>Camellia sinensis Tea South-east Asia, possibly. Cultivated from tropical to temperate</p><p>zones. Grows as bushes and, unlike other woody perennials, the</p><p>leaves constitute the product</p><p>Carica papaya Papaya Lowlands of Central America and southern Mexico. Pantropical.</p><p>A fast and highly productive species, usually short-lived, but</p><p>can produce fruits for more than 20 yr. Can reach 10 m height</p><p>Citrus spp. Include varieties</p><p>of oranges, grape-</p><p>fruit, lemons and</p><p>limes</p><p>Obscure; most cultivated species appear to be indigenous to the</p><p>more humid tropical or near-tropical regions of China and</p><p>South-east Asia; some authors have classified citrus as</p><p>subtropical species. Widely cultivated in most tropical and</p><p>subtropical zones. Do not tolerate freezes</p><p>Cocus nucifera Coconut Southeast Asia. Limited to tropical lowlands, between 20oN and</p><p>20oS. A palm that grows in sunny and humid environments</p><p>Coffea arabica Arabica coffee Ethiopian highland tropical forest. Tropical highlands. Evolved</p><p>as understory tree but open plantations generally produce more</p><p>than shade plantations under high-input systems</p><p>Coffea canephora Robusta coffee Congo basin rainforest. Tropical lowland areas. Accounts for</p><p>34% of the world's coffee production. Together with arabica</p><p>coffee, constitutes the second most valuable traded commodity</p><p>worldwide</p><p>Elaeis guineensis Oil palm Tropical forests of West and Central Africa. Widely grown in</p><p>humid equatorial lowlands; growth is very slow below 20oC.</p><p>The most productive crop for plant oil</p><p>Hevea brasiliensis Rubber Amazonian tropical rainforest. Traditionally cultivated between</p><p>10oN and 10oS. Cultivation has been presently expanded</p><p>towards higher latitudes. Latex constitutes the product</p><p>Mangifera indica Mango Northeastern India. Throughout tropics and subtropics. Can</p><p>tolerate a relatively wide temperature range. Maximum mango</p><p>yield is relatively low compared with other tree fruit crops</p><p>Manihot esculenta Cassava American origin, possibly from northeastern Brazil. Pantropical.</p><p>High-yielding woody shrub grown as annual or biennial for its</p><p>starchy roots before becoming fibrous. Unmanaged plants</p><p>behave as small trees reaching about 5 m height</p><p>Musa spp. Banana Tropical southeast Asia. Pantropical. High-yielding perennial</p><p>crop reaching up to 8 m height. Thoroughly entwined in cultures</p><p>throughout the tropics and seen as ideal for agroforestry</p><p>schemes.</p><p>Theobroma cacao Cacao Central and western Amazon. Warm and humid tropics. Grows</p><p>generally under shade with very low productivity. It is almost</p><p>exclusively explored for chocolate manufacturing</p><p>Introduction</p><p>3</p><p>Plants are frequently exposed to a variety of harsh environmental conditions that</p><p>negatively affect crop growth and yield. An understanding of the responses of crops to their</p><p>environment is thus fundamental to minimize the deleterious impact of unfavorable climatic</p><p>conditions and to manage crops for maximum productivity. Boyer (1982), for instance, has</p><p>argued that water supply affects the productivity of trees and annual crops more than all other</p><p>environmental factors combined. This aspect has been deeply explored in this book for</p><p>banana, cassava, coconut, papaya, and tea; however, the development of an internal water</p><p>deficit may be important to some crops such as coffee and mango in order to trigger</p><p>phenological events such as flower bud release. Decreases in yield induced by low a soil</p><p>water supply may largely be associated with a decline in photosynthetic rates, either by a</p><p>direct effect of dehydration on the photosynthetic apparatus or by an indirect effect such as</p><p>stomatal closure, which restricts CO2 uptake. In addition to soil water deficits, atmospheric</p><p>water deficit is also of particular relevance to tropical tree crops. This is due to the very low</p><p>root hydraulic conductivity as compared with annuals, which brings about a pronounced</p><p>transpiration effect on tree-water relations (DaMatta, 2003). Furthermore, for a tropical</p><p>environment the range of evaporative demand in average is far higher than for temperate</p><p>zones. This implies that leaf water status changes much more diurnally in tropical trees than</p><p>in many temperate trees or annuals, and leaf water deficits may occur under the high</p><p>evaporative demand even without any soil water shortage, such as in banana, cocoa, coffee,</p><p>papaya, and tea. Therefore, regulation of leaf water status by atmospheric conditions is</p><p>relatively more important in tropical tree crops than in many other crops. The yield of crop</p><p>plants under soil and/or atmospheric drought stress will largely depend on adaptive</p><p>mechanisms allowing them to maintain growth and high photosynthetic production under</p><p>prolonged</p><p>of vegetative and</p><p>reproductive growth in cocoa grown in controlled glasshouse conditions. Proceedings of</p><p>the 11th international cocoa research conference. Yamoussoukro; 1994. p.319-31.</p><p>Hardwick K, Baker NR, Bird KJ. 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Syst. 2005;84:195-225.</p><p>In: Ecophysiology of Tropical Tree Crops ISBN 978-1-60876-392-4</p><p>Editor: Fabio DaMatta © 2010 Nova Science Publishers, Inc.</p><p>Chapter 4</p><p>CASSAVA: PHYSIOLOGICAL MECHANISMS AND</p><p>PLANT TRAITS UNDERLYING TOLERANCE TO</p><p>PROLONGED DROUGHT AND THEIR APPLICATION</p><p>FOR BREEDING IMPROVED CULTIVARS IN THE</p><p>SEASONALLY DRY AND SEMIARID TROPICS</p><p>Mabrouk A. El-Sharkawy</p><p>ABSTRACT</p><p>This chapter summarizes research conducted at International Center for Tropical</p><p>Agriculture (CIAT) on responses of cassava (Manihot esculenta Crantz) to extended</p><p>water shortages in the field aided by modern gas-exchange, water-relation techniques and</p><p>biochemical assays. The aim of the research was to coordinate basic and applied aspects</p><p>of crop physiology into a breeding strategy with a multidisciplinary approach. Several</p><p>physiological characteristics/traits</p><p>and mechanisms underpinning tolerance of cassava to</p><p>drought were elucidated using a large number of genotypes from the CIAT core</p><p>germplasm collection grown in various locations representing ecozones where cassava is</p><p>cultivated. Most notable among these characteristics are the high photosynthetic capacity</p><p>of cassava leaves in favorable environments and the maintenance of reasonable rates</p><p>throughout prolonged water deficits, a crucial characteristic for high and sustainable</p><p>productivity. Cassava possess a tight stomatal control over leaf gas exchange that reduces</p><p>water losses when plants are subjected to soil water deficits as well as to high</p><p>atmospheric evaporative demands. During prolonged water deficits, cassava reduces its</p><p>canopy by shedding older leaves and forming smaller new leaves leading to less light</p><p>interception. Though root yield is reduced (but much less than the reduction in top</p><p>growth) under water deficit, the crop can recover when water becomes available by</p><p>rapidly forming new canopy leaves with much higher photosynthetic rates compared to</p><p>unstressed crops. Cassava can extract slowly water from deep soils, a characteristic of</p><p>paramount importance in seasonally dry and semiarid environments where deeply stored</p><p>water needs to be tapped. Screening large accessions under seasonally dry and semiarid</p><p>environments showed that yield is significantly correlated with upper canopy leaf</p><p>photosynthetic rates, and the association was attributed mainly to nonstomatal</p><p>Mabrouk A. El-Sharkawy</p><p>72</p><p>(anatomical/biochemical) factors. Parental materials with both high yields and</p><p>photosynthetic rates were identified for incorporation into breeding and selection</p><p>programs for cultivars adapted to prolonged drought coupled with high temperatures and</p><p>dry air, conditions that might be further aggravated by global climate changes in tropical</p><p>regions.</p><p>INTRODUCTION</p><p>The role of physiological research in crop improvement and cropping systems</p><p>management has recently been reviewed (El-Sharkawy, 2006b). As a branch of basic science,</p><p>plant physiological research has a fundamental role in advancing the frontier of knowledge</p><p>that is essential for the better understanding of plants and their interactions with surrounding</p><p>biophysical environments. It also plays a significant role in supporting other branches of</p><p>science that deal with the practical application of knowledge and in the development of</p><p>advanced technologies needed for improving biological systems in general and agricultural</p><p>productivity in particular. Crop physiology deals with studying cultivated crops with the aim</p><p>of increasing productivity by enhancing the inherent genetic capacities of crops as well as</p><p>their adaptability to environments. To be effective in realizing such a goal, physiologists have</p><p>to work within multidisciplinary research teams committed to a particular crop and/or to</p><p>multi-cropping systems (Nguyen and Blum, 2004; El-Sharkawy, 2005; Sawan et al., 2005;</p><p>Long et al., 2006; Begonia and Begonia, 2007; Steiner and Hatfield, 2008; Yin and Struik,</p><p>2008). Furthermore, to be successful, the leader/manager of a multidisciplinary research team</p><p>should not tolerate potential rivalries between disciplines involved nor the dominance of a</p><p>particular discipline for research support and funds (El-Sharkawy, 2005). Funding agencies</p><p>for research and development should encourage, and perhaps urge, long-term projects based</p><p>on interdisciplinary/interinstitutional collaborative research spanning from genomics to agro-</p><p>ecosystems levels in order to increase the benefit/cost ratio as well as the effectiveness and</p><p>wide applicability of improved technologies, as was the case in the 1960’s Green Revolution</p><p>based on development of semi-dwarf high yielding cereal varieties with associated improved</p><p>cultural practices (Wortman, 1981; Borlaug, 1983). Borlaug (1983) and El-Sharkawy (2006b)</p><p>emphasized the role of conventional plant breeding and physiological research, respectively,</p><p>in crop improvement and cautioned against the current trends in research funding system that</p><p>overemphasized the genetic engineering approach at the expense of other research disciplines.</p><p>Borlaug (1983) stated that “since it is doubtful that significant production benefits will soon</p><p>be forthcoming from the use of genetic engineering techniques with higher plants, especially</p><p>polyploidy species, most research funds for crop improvement should continue to be allocated</p><p>for conventional plant breeding research”. Nevertheless, there is no doubt that more recent</p><p>advances in molecular biology research, and associated genetic engineering technology, have</p><p>enhanced the scientific knowledge-base and also partially have led to crop improvement via</p><p>producing pest-and-herbicide-resistant crop cultivars now widely cultivated across continents,</p><p>although there are some concerns about their bio-safety for humans, animals, natural and</p><p>managed ecosystems (Brown, 1983; Mazur and Falco, 1989; Hilbeck, 2001). Another area</p><p>promising contribution of “exotic” gene-transfer to food crops is the ongoing work to</p><p>improve the nutritional quality of major staple food crops such as rice (e.g. Potrykus, 1991).</p><p>Having said that, I would like to further qualify Borlaug’s statement by recommending a more</p><p>Cassava</p><p>73</p><p>balanced approach in research funding and support so that all disciplines within the domain of</p><p>national and international agricultural research systems can be fully exploited in enhancing</p><p>agricultural productivity and at the same time ensure a safe environment via sound integrative</p><p>production management.</p><p>Although research conducted in laboratories and in controlled environments is useful in</p><p>elucidating a specific plant physiological characteristic or mechanisms underlying certain</p><p>biological processes and responses to environmental factors affecting growth and</p><p>productivity, by themselves they are inadequate for creating some benefit to the farmer</p><p>(Kramer, 1980, 1981; Evans et al.,1985). Field research under representative environments</p><p>and in relevant cropping systems using a broad genetic base must be conducted not only to</p><p>verify findings in laboratories and controlled environments but also to generate essential</p><p>information and insights concerning the real potential of crops under natural conditions as</p><p>well as their responses to a specific limiting environmental factor (El-Sharkawy et. al, 1965;</p><p>El-Sharkawy 1993, 2004, 2005, 2006a, 2006b; Sawan et al., 2002; Long et al., 2006; Steiner</p><p>and Hatfield, 2008). El-Sharkawy (2004, 2005, 2006a, 2006b) and Long et al. (2006) have</p><p>shown that research based only on potted plants grown in greenhouses and in controlled</p><p>cabinets, without the proper calibration in the field, is a waste of time and resources since in</p><p>most cases results cannot be extrapolated, or simulated by crop modeling, to describe what</p><p>may take place in natural environments. Those authors concluded that field research is the</p><p>only valid ecosystem research in studying plant water relations and crop photosynthesis in</p><p>relation to productivity.</p><p>Until three decades ago, crops other than wheat, rice and maize, were not included in the</p><p>research agenda of the first two commodity-oriented international agriculture research</p><p>centers, i.e. the International Rice Research Institute (IRRI) in the Philippines and the</p><p>International Maize and Wheat Improvement Center (CIMMYT, from the Spanish acronym)</p><p>in Mexico (Wortman, 1981). This situation was largely corrected by the creation of more</p><p>international research laboratories and centers in Africa, Asia and Latin America dealing with</p><p>various crops, ecosystems and natural resources management. The International Center for</p><p>Tropical Agriculture (CIAT, from the Spanish acronym) in Colombia has a world mandate for</p><p>research on cassava, while the International Institute of Tropical Agriculture (IITA) in</p><p>Nigeria has a more regional mandate. Since then, research on cassava has received</p><p>attention</p><p>and support from many developed countries and from various research/development granting</p><p>agencies.</p><p>The cassava plant is a perennial shrub (see Figure 1) that under natural and unmanaged</p><p>agricultural systems behaves as a small tree with thick fibrous roots and reaching heights</p><p>greater than 3 m. It is native to the Americas and may have been domesticated before 4000</p><p>BC (Ugent et al., 1986; Allem, 2002). It is cultivated as an annual and biennial crop for its</p><p>starchy roots (approximately 85% starch on DW basis) that could be harvest at 8 to 18 months</p><p>after planting. After the conquest of the Americas, cassava was first introduced to Africa in</p><p>the sixteenth century and later to Asia in the seventeenth century. Today, the crop had</p><p>become the fourth most important source of calories (after rice, sugarcane, and maize) for</p><p>more than 500 million people throughout tropical Africa, Asia, and Latin America. Current</p><p>world production exceeds 200 million tons of fresh roots (more than half of it comes from</p><p>Africa), with an average yield around 10 t ha-1. In contrast with the capital-intensive Green</p><p>Revolution technology, cassava is produced mainly by small farmers who do not rely on</p><p>purchased inputs.</p><p>Mabrouk A. El-Sharkawy</p><p>74</p><p>Figure 1. Typical cassava plantations growing in semiarid Brazil. Courtesy of Dr. Luciano da Silva</p><p>Souza – Embrapa Mandioca e Fruticultura Tropical (Brazil).</p><p>The majority of cassava production occurs in marginal, low-fertility acid soils with</p><p>annual rainfall that ranges from less than 600 mm in the semiarid tropics to more than 1500</p><p>mm in the subhumid and humid tropics (El-Sharkawy, 1993; Hillocks et al., 2002). More than</p><p>70% of cassava storage roots is used for human food either in fresh form after cocking of</p><p>varieties low in hydrocyanic acid (HCN) (i.e. sweet varieties) and in processed form of</p><p>varieties high in HCN (bitter varieties). The remaining production is used for animal feed and</p><p>for starch extraction. In some African countries, young leaves low in HCN are also consumed</p><p>as human food in various recipes after pounding and cooking (Lancaster and Brooks, 1983;</p><p>Ufuan Achidi et al., 2005).</p><p>Before CIAT, with a very few exceptions, cassava was a neglected crop as far as research</p><p>was concerned in tropical countries. Physiological information on cassava was, until recently,</p><p>scarce (Hunt et al., 1977; Cock et al., 1979; Cock, 1985; Splittstoesser and Tunya, 1992; El-</p><p>Sharkawy, 1993). The cassava physiology section at CIAT conducted both basic and applied</p><p>research in coordination with a breeding program and took advantage of the diverse genetic</p><p>resources available within the extensive cassava germplasm collection as well as the diverse</p><p>environments within Colombia where cassava is cultivated (El-Sharkawy, 1993; Madeley,</p><p>1994). The research covered a wide range of ecophysiological aspects of the crop. Cassava</p><p>was the first cultivated crop to be considered as a C3-C4 intermediate species based on: (i)</p><p>atypical leaf anatomy including the presence of conspicuous thin-walled bundle-sheath cells</p><p>with large granal chloroplasts, which are less developed than those in the typical C4 Kranz</p><p>leaf anatomy (e.g., El-Sharkawy and Hesketh,1965, 1986; Laetsch, 1974); (ii) close physical</p><p>association of chloroplasts with numerous mitochondria and peroxisomes in bundle-sheath</p><p>and mesophyll cells; (iii) low photorespiration (as determined by CO2 release from</p><p>illuminated leaves in a rapid stream of CO2-free air, less than 10% of net photosynthesis) and</p><p>low CO2 compensation point (Г = 20-30 cm3 m-3); (iv) ability to recycle all internal</p><p>respiratory CO2 within the palisade layer when abaxial stomata of amphistomatous leaves are</p><p>closed under a wide range of irradiances and temperatures; (v) elevated activities of the C4</p><p>phosphoenolpyruvate carboxylase (PEPC) in leaf extracts (10-30% of activities in maize and</p><p>sorghum); (vi) high percentage (30-60%) of 14C labeling in C4 dicarboxylic acids after 5-10 s</p><p>Cassava</p><p>75</p><p>exposure under illumination; (vii) and immunological analysis and DNA hybridization of</p><p>PEPC from cassava and wild Manihot species against antibodies and ppc probes from maize</p><p>(El-Sharkawy and Cock, 1987a; Cock et al., 1987; Riaño et al., 1987a, 1987b; El-Sharkawy et</p><p>al. 1989, 2008; El-Sharkawy and Cock, 1990; Bernal, 1991; López et al., 1993; Aguilar,</p><p>1995; El-Sharkawy, 2004, 2006a; El-Sharkawy and de Tafur, 2007). These characteristics,</p><p>collectively, underpinned the high rate of net photosynthesis (A) in normal air (> 40 µmol</p><p>CO2 m-2 s-1) in high irradiances (> 1800 µmol m-2 s-1 of PAR), high leaf temperature from 30</p><p>to 40○C, and in high atmospheric humidity observed in cassava grown in favorable</p><p>environments (El-Sharkawy et al., 1992a, 1993).</p><p>Moreover, leaf A, as measured in the field, was significantly correlated with both total</p><p>biomass and root yield of a wide range of cultivars grown across years and environments. The</p><p>relations were attributed mainly to nonstomatal (biochemical/anatomical) factors (El-</p><p>Sharkawy, 2004, 2006a). Cassava also tolerates prolonged drought that often exceeded five</p><p>months aided by partial closure of stomata, deep rooting systems and small leaf canopy.</p><p>These plant traits make cassava a desirable and adaptable crop, as source for food and feed, in</p><p>the tropical regions that would be adversely affected by global climate changes (Rosenzweig</p><p>and Parry, 1994; Kamukondiwa, 1996; El-Sharkawy, 2005; IPCC, 2006).</p><p>This chapter summarizes some research findings, published and unpublished, on the</p><p>responses of cassava to extended water shortages in the field where physiological</p><p>mechanisms and characteristics related to the crop’s tolerance to drought were sorted out.</p><p>Moreover, the research laid the foundations for selection and breeding of improved cultivars</p><p>adapted to prolonged drought normally encountered in seasonally dry and semiarid</p><p>environments.</p><p>RESEARCH AT CIAT ON CASSAVA RESPONSES TO EXTENDED</p><p>WATER SHORTAGES</p><p>Responses to Prolonged Mid-Season Water Deficit</p><p>Research at CIAT (Connor et al., 1981; Porto, 1983; El-Sharkawy and Cock, 1987b) has</p><p>shown that cassava tolerates a relatively long period of drought once the crop is established.</p><p>In these studies, using a limited number of varieties, a stress period of 2-3 months was</p><p>imposed 3-4 months after planting. The crop was later allowed to recover from stress for the</p><p>rest of the growing cycle with the aid of rainfall and supplementary irrigation.</p><p>Figure 2 presents the relationship of yield with the seasonal average leaf area index (LAI)</p><p>for four contrasting varieties, as affected by a prolonged mid-season water stress conducted in</p><p>two separate field trials (El-Sharkawy and Cock, 1987b). The highest reference (100%) yields</p><p>were 19 t ha-1 dry root for ‘CM 507-37’ under non-stressed conditions over 345 d in</p><p>Experiment I (El-Sharkawy and Cock, 1987b) and 11.2 t ha-1 for ‘M Col 22’ under non-</p><p>stressed conditions for 306 d in Experiment II (Connor et al., 1981). Compared with the</p><p>control, the final root yields of the stressed crop were increased in vegetative vigorous</p><p>varieties (e.g. ‘M Mex 59’); were reduced in less vigorous types (e.g. ‘M Col 22’); and</p><p>slightly reduced or remained unchanged in varieties with intermediate vigor (e.g. the parent</p><p>‘M Col 1684’ and the its hybrid ‘CM 507-37’). These responses were closely related to leaf</p><p>Mabrouk A. El-Sharkawy</p><p>76</p><p>area characteristics (i.e. peak LAI and leaf area duration over the growing cycle), and to</p><p>patterns of photoassimilate partitioning between top growth (stems and leaves) and storage</p><p>roots. The vigorous types responded positively to stress because top growth was reduced and</p><p>the harvest index (HI) was increased, whereas the less vigorous types responded negatively</p><p>because leaf area was drastically reduced to levels below optimal LAI for root yield (El-</p><p>Sharkawy and Cock, 1987b). The stability of root yields in intermediate types under both</p><p>favorable</p><p>and stressful environments stemmed from an ability to maintain leaf area near</p><p>optimum during a major part of the growing cycle. Also, the relationship between leaf area</p><p>and storage root yield is very important when cassava is subjected to a cold period coupled</p><p>with water shortages in the subtropics where leaf area is reduced. Under these conditions, the</p><p>crop requires a second warm-wet cycle for leaf area recovery and for attaining higher yields</p><p>(Sagrilo et al., 2006). A similar ideotype approach was followed in studying tolerance to</p><p>water and heat/cold stresses in various crops including winter and spring wheat, maize,</p><p>sorghum, millets, cowpea and coffee (Kirkham, 1980, 1988; Kirkham et al., 1984; Blum and</p><p>Pnuel, 1990; Bolaños and Edmeades, 1993a, 1993b; Bolanños et al., 1993; Whan et al, 1993;</p><p>Richards, 2000; DaMatta and Ramalho, 2006). This information on the mode of response to</p><p>water shortages is fundamental for a cassava breeding strategy and points to the need for</p><p>selecting different plant types for different environments, a strategy later adopted by CIAT</p><p>and IITA, (Hershey and Jennings 1992; El-Sharkawy, 1993; Iglesias et al., 1995; Iglesias and</p><p>Brekelbaum, 1996) and by national cassava programs, as in Brazil (Fukuda et al., 1992-1993).</p><p>Figure 2. Dry root yield as a function of growth cycle average leaf area index (LAI) under non-stress</p><p>and midterm water stress conditions for four cultivars with different vigor. Data of experiment I for</p><p>‘CM 507-37’ and ‘M Col 1684’ from El-Sharkawy and Cock (1987b); data of experiment II for ‘M Col</p><p>22’ and ‘M Mex 59’ from Connor et al. (1981). From El-Sharkawy and Cock (1987b). Permission</p><p>conveyed through Copyright Clearance Center, Inc.</p><p>Cassava</p><p>77</p><p>Nevertheless, CIAT researchers needed to know to what extent cassava can tolerate a</p><p>more prolonged period of water deficit imposed at an earlier stage of growth. They also</p><p>needed to simulate, as closely as possible, the common cassava-farming practice of planting</p><p>cassava near the end of a rainy season, letting it pass through a long period of no rain, and</p><p>then allowing it to recover in a second wet cycle. This objective was addressed using larger</p><p>group of varieties.</p><p>Responses to Prolonged Early Water Deficit</p><p>In the 1987-1988 season, eight cassava varieties (Table 1) were planted on 25 November</p><p>1987, in a field drainage lysimeter (30 m x 15 m x 2.30 m deep) that was constructed in 1981</p><p>by excavating the soil layer by layer to 2.5 m where bottom ground was compacted and</p><p>covered with 0.3 cm layer of black asphalt, then 15 cm layers of sand and gravel, and</p><p>perforated plastic tubes were installed at narrow distances to collect drainage water into a</p><p>nearby reservoir (Porto, 1983; El-Sharkawy and Cock, 1987b). The separately-excavated soil</p><p>layers were then returned back to their original depths and were compacted manually to have</p><p>their bulk densities near the original values. Plants were adequately fertilized and the plots</p><p>were kept weed-free manually. Because of rainfall deficits in December 1987 (94 mm) and</p><p>January 1988 (81 mm), three irrigations were applied to ensure cassava sprouting and</p><p>establishment. Two months after planting, before imposing the stress, supplementary</p><p>irrigation was applied to bring the soil-water content (SWC) to near field capacity within the</p><p>2.3-m soil depth. The available SWC within the 2.3-m profile of the experimental site was</p><p>about 250 mm (between -0.03 and -1.5 MPa). Half of the experimental area was covered with</p><p>white plastic sheets to exclude rainfall from day 60 to day 180 after planting. At this stage of</p><p>growth, cassava had less than 0.8 LAI and less than 2 t ha-1 total dry biomass, with no visible</p><p>storage roots (Connor et al., 1981; Porto, 1983; CIAT, 1987-1989; El-Sharkawy and Cock,</p><p>1987b; Pellet and El-Sharkawy, 1993, 1997). During the stress period of four months, the</p><p>control plot received about 540 mm of rain, together with three heavy irrigations within the</p><p>first and second month, to compensate for the rainfall deficits in that period. The total amount</p><p>of water received by the control plot in four months was greater than the potential</p><p>evapotranspiration at the Quilichao Experiment Station (about 4.2 mm d-1). In the stressed</p><p>plots, water was removed manually immediately after rainfalls and any cracks in the plastic</p><p>sheets were sealed. The plastic cover was removed during the first week of June 1988. By the</p><p>end of the stress period, the total water extracted from 2.3 m soil depth ranged among</p><p>varieties from 168 to 200 mm. From 1 June to 20 October, the total rainfall was 656 mm.</p><p>Supplementary irrigation to both the stressed and control plots was applied twice in June,</p><p>July, and August to compensate for the low rainfall during that period. The total rainfall</p><p>received from planting to harvest was 1406 mm in the control and 865 mm in the stressed</p><p>plots.</p><p>Table 1. Final yields and biomass of eight cassava cultivars as affected by an early and prolonged period of water stress. From day 60 to</p><p>180 after planting, plants were deprived of rainfall and then were allowed to recover under irrigation and rainfall for the rest of the</p><p>growth cycle. Rainfall was excluded by covering the soil of the stresses plot with plastic sheets. The experiment was conducted at</p><p>Santander de Quilichao, Cauca, Colombia; the planting date was 25 November 1987, and the cassava was harvested on 20 October 1988.</p><p>From CIAT (1987-1989)</p><p>Cultivar Control Stress</p><p>Dry Fresh Dry Dry Harvest Dry Fresh Dry Dry Harvest</p><p>biomass yield yield matter index biomass yield yield matter Índex</p><p>in roots in roots</p><p>t ha-1 % t ha-1 %</p><p>‘M Col 1684’ 27.0 50.5 16.9 33.5 63 18.2 41.8 13.9 33.1 76</p><p>‘CM 489-1’ 26.4 59.6 18.8 31.6 71 26.8 59.0 17.5 29.6 65</p><p>‘CM 507-37’ 22.6 42.2 14.1 33.3 62 24.0 52.6 17.2 32.6 72</p><p>‘CM 523-7’ 25.8 42.7 16.3 38.2 63 26.9 45.6 17.4 38.2 65</p><p>‘CM 922-2’ 24.8 42.7 16.9 39.4 68 26.0 44.3 17.0 38.3 65</p><p>‘CM 1335-4’ 29.8 51.6 20.2 39.3 68 26.5 51.0 19.1 37.5 72</p><p>‘CM 2136-2’ 38.0 58.7 20.9 35.5 55 27.7 55.4 17.3 31.1 62</p><p>‘CM 3306-32’ 33.8 41.3 15.2 36.7 45 24.5 41.1 15.2 37.0 62</p><p>Average 28.5 48.7 17.4 35.9 61 25.1 48.9 16.8 34.7 67</p><p>Difference due -12 0.0 -3.4 -3.3 +10</p><p>to stress (%)</p><p>LSD (P = 0.05) 3.1 4.5 2.0 3.9 5 2.3 4.1 1.8 3.7 6</p><p>Note: The small reduction in dry root yield was due mainly to reduction in dry matter contents of roots. The larger reduction in total biomass was attributed to a</p><p>larger reduction in shoot biomass, compared to reduction in storage roots, and hence, a higher harvest index under stress.</p><p>Cassava</p><p>79</p><p>During the stress period, field measurements of leaf gas exchange were made with a</p><p>portable infrared CO2 analyzer on single, attached, upper canopy leaves at solar radiation</p><p>greater than 1000 µmol m-2 s-1 of PAR. These measurements were normally made between</p><p>0900 and 1300 h once a week within the first two months, and once every two weeks within</p><p>the last two months of stress. Light interception, leaf water potential (Ψw), and SWC were</p><p>also monitored. Final harvest was made on 20 October 1988 (11 months after planting) and</p><p>the total standing biomass, root yield and dry matter contents of roots were determined.</p><p>Table 1 summarizes data of final standing total biomass, root yields, HI, and dry matter</p><p>contents of storage roots. In the control plot, the total dried biomass ranged (in round figures)</p><p>among varieties from 23 to 38 t ha-1, fresh roots from 42 to 60 t ha-1, dried roots from 14 to 21</p><p>t ha-1; dry matter contents from 32% to 39%; and HI from 45% to 71%. In the stressed plot,</p><p>the ranges were (again in round figures) 18 to 28 t ha-1 for total biomass, 41 to 59 t ha-1 for</p><p>fresh roots, 14 to 19 t ha-1 for dried roots, 30% to 38% for dry matter contents, and 62% to</p><p>76% for HI.</p><p>There were notable varietal differences in response to stress. Fresh and dried-root yields</p><p>were</p><p>decreased by stress in the parent ‘M Col 1684’, whereas they increased in its hybrid</p><p>‘CM 507-37’. Previous studies with these two genetically related varieties (‘CM 507-37’ is a</p><p>hybrid between ‘M Col 1684’ and ‘M Col 1438’) have shown that ‘CM 507-37’ is more</p><p>vegetative vigorous and leafy (El-Sharkawy and Cock, 1987b, El-Sharkawy et al., 1992b). In</p><p>other varieties, the yields were relatively unchanged, except for ‘CM 2136-2’, where dried-</p><p>root yields decreased notably, mainly because of reduction in dry-matter contents from 35.5%</p><p>to 31.1%.</p><p>Compared with the control, water deficit across all varieties caused a reduction in total</p><p>biomass by 12%, no change in fresh root yields, a reduction in dried-root yields by 3.4%, a</p><p>reduction in dry matter contents by 3.3%, and an increase in HI by 10%. These data clearly</p><p>demonstrate cassava’s ability to tolerate prolonged drought when it is induced gradually at an</p><p>early stage of growth. Furthermore, the crop is able to recover and compensate, in terms of</p><p>economic yields, from the adverse effects of stress. In areas with intermittent rainfall and with</p><p>long periods of drought, cassava should produce reasonably well, providing good crop</p><p>management (e.g. weed control and adequate fertilization) is practiced and cassava is grown</p><p>in deep soils with good water-holding capacity.</p><p>The physiological mechanisms that underlie cassava’s tolerance of severe water deficit</p><p>are illustrated by data in Tables 2 and 3 and Figures 3, 4 and 5. The capacity of cassava leaves</p><p>to fix atmospheric CO2, a basic process for dry matter accumulation, during the stress period</p><p>was 80% of that in the control (Table 2, Figure 3). This indicated that the photosynthetic</p><p>process in cassava is not greatly inhibited by prolonged stress, an advantage that many other</p><p>field crops do not have. A second and important physiological mechanism of cassava leaves</p><p>is their ability to partly close their stomata in response to water stress. For example, in the</p><p>experiment, there was an average 43% reduction in stomatal conductance to water vapor (gs)</p><p>in stressed plots (Table 2) and consistent reduction over the stress period, compared to the</p><p>control (Figure 4). The partial closure of stomata enabled cassava leaves to maintain, to some</p><p>extent, the midday leaf Ψw at levels comparable with those of cassava leaves in the control</p><p>plot. Leaf Ψw at 1400 h across all varieties was about -1.13 MPa regardless of water supply</p><p>(Table 3). This is another comparative advantage for cassava in dry areas, compared to other</p><p>crops with poorer stomatal control. In addition to its beneficial effect by preventing severe</p><p>Mabrouk A. El-Sharkawy</p><p>80</p><p>leaf dehydration, and consequently preventing impairment to photosynthetic capacity of the</p><p>leaf, the partial closure of stomata reduces water loss through transpiration (Figure 5), thereby</p><p>maximizing water-use efficiency, WUE (i.e. the amount of CO2 fixed per amount of water</p><p>transpired). Across all varieties, there was 39% increase in intrinsic leaf WUE (A/gs) in</p><p>stressed plants over the control (Table 2).</p><p>Table 2. Leaf net photosynthetic rate (A) (μmol CO2 m-2 s-1), stomatal conductance to</p><p>water vapor diffusion (gs) (mmol m-2 s-1), mesophyll conductance to CO2 diffusion (gm)</p><p>(mmol m-2 s-1), and irradiance interception (I) (%)of eight cassava cultivars as affected</p><p>by an early and prolonged period of water stress. The A/gs ratio (mmol mol-1) indicates</p><p>the average leaf intrinsic water-use efficiency. Values are means of all measurements</p><p>made during the stress period from day 60 to day 180 after planting. Measurements</p><p>were made weekly for the first two months and every two weeks in the last two months</p><p>of stress (12 measurements x three replications). From CIAT (1987-1989)</p><p>Cultivar Control Stress</p><p>A gs gm I A gs gm I</p><p>‘M Col 1684’ 21.4 815 85 64 18.0 485 76 46</p><p>‘CM 489-1’ 25.6 1001 104 58 19.6 557 89 37</p><p>‘CM 507-37’ 23.1 940 92 62 17.3 515 72 45</p><p>‘CM 523-7’ 24.1 937 97 68 16.2 440 69 42</p><p>‘CM 922-2’ 25.8 992 102 58 22.3 553 99 37</p><p>‘CM 1335-4’ 20.6 833 82 61 18.2 565 77 50</p><p>‘CM 2136-2’ 26.2 1033 104 65 20.6 606 86 37</p><p>‘CM 3306-32’ 24.9 850 101 63 17.8 492 78 51</p><p>LSD (P = 0.05) 2.1 97 11 NS 1.8 67 9 6</p><p>Average of</p><p>all cultivars 24 925 96 62 19 527 81 43</p><p>Difference due to stress (%) -21 -43 -16 -31</p><p>A/gs 0.026 0.036</p><p>NS, non-significant; P > 0.05.</p><p>Note: The larger reduction in gs than in A under stress resulted in ca. 39% increase in leaf intrinsic</p><p>water-use efficiency. The reduction in irradiance interception under stress was attributed mainly to</p><p>smaller leaf canopy (i.e. lower LAI). Under stress small-sized new leaves are formed at a slower</p><p>rate, compared to unstressed crop. Since under stress harvest index increases (see Table 1),</p><p>reduction in irradiance interception will lead to less crop transpiration rate, and hence, to greater</p><p>crop water-use efficiency in terms of storage root production. Moreover, when stressed plants</p><p>recover in wet conditions, they rapidly form new leaf canopy with even higher leaf A than those in</p><p>unstressed leaves, thus final yield approaches values obtained in well-watered plants (see Tables 1,</p><p>4; El-Sharkawy and Cock, 1987b; El-Sharkawy et al., 1992b, 1998; El-Sharkawy, 1993, 2006a;</p><p>Cayón et al., 1997; El-Sharkawy and Cadavid, 2002). Under prolonged drought (> 5 months) in</p><p>semiarid environments with less than 500 mm of effective annual rainfall, cassava survives and</p><p>produces reasonable yields (3 to 5 t DM ha-1 with improved cultivars) which can be greatly</p><p>increased (2-3 times) with a second cycle of rainfall (see Tables 7 and 8).</p><p>Cassava</p><p>81</p><p>Figure 3. Response of cassava leaf photosynthesis to prolonged water stress (120 d), imposed at 60 d</p><p>after planting (control, open symbols; stress, solid symbols). From CIAT (1987-1989) Report.</p><p>Mabrouk A. El-Sharkawy</p><p>82</p><p>Figure 4. Response of cassava stomata to prolonged water stress (120 d), imposed at 60 d after planting</p><p>(control, open symbols; stress, solid symbols). From CIAT (1987-1989) Report.</p><p>A third and equally important physiological mechanism that enables cassava to withstand</p><p>severe water stress is its ability to maintain a leaf predawn Ψw comparable with that of</p><p>unstressed cassava. In the experiment, leaf Ψw at 0600 h across all varieties was about -0.40</p><p>MPa irrespective of watering treatments (Table 3). This was partly achieved by reducing total</p><p>leaf area (as indicated by the 31% reduction in light interception in the stressed plot; Table 2),</p><p>thereby reducing total canopy transpiration rate (E), and by slow withdrawal of water from</p><p>the deeper layers of the soil profile (Figure 6) (Connor et al., 1981; Porto 1983; CIAT, 1987-</p><p>Cassava</p><p>83</p><p>1989; El-Sharkawy and Cock, 1987b; El-Sharkawy et al., 1992b; de Tafur et al., 1997a;</p><p>Cadavid et al., 1998; El-Sharkawy, 2006a). During water stress, cassava fine roots extend for</p><p>more than 2 m into deeper, wetter soil from where cassava can extract between 20% and 40%</p><p>of its total water uptake (CIAT, 1987-1989; El-Sharkawy et al., 1992b). This is of paramount</p><p>importance in areas with bimodal rainfall patterns and those with one short-wet annual period</p><p>where excess water percolates deeper in soil profile and, hence, it could be extracted during</p><p>long dry periods.</p><p>Figure 5. Response of cassava leaf transpiration to prolonged water stress (120 d), imposed at 60 d after</p><p>planting (control, open symbols; stress, solid symbols). From CIAT (1987-1989) Report.</p><p>Table 3. Leaf water potential (-MPa) of eight cassava cultivars measured from 0600 to 1400h as affected by an early and prolonged</p><p>period of water stress. Values are means of all measurements made during the stress period from day 60 to day 180 after planting.</p><p>Measurements were made with the pressure chamber technique weekly for the first two months and every two weeks in the last two</p><p>months of stress (12 measurements x three replications). From</p><p>CIAT (1987-1989)</p><p>Cultivar Control plants Stressed plants</p><p>0600 h 0800 h 1100 h 1400 h 0600 h 0800 h 1100 h 1400 h</p><p>‘M Col 1684’ 0.38 0.69 0.99 1.07 0.40 0.80 1.02 1.07</p><p>‘CM 489-1’ 0.38 0.76 1.05 1.10 0.41 0.83 1.09 1.15</p><p>‘CM 507-37’ 0.38 0.79 1.08 1.19 0.39 0.88 1.16 1.18</p><p>‘CM 523-7’ 0.40 0.77 1.04 1.09 0.39 0.83 1.06 1.09</p><p>‘CM 922-2’ 0.39 0.75 0.98 1.11 0.42 0.87 1.05 1.12</p><p>‘CM 1335-4’ 0.38 0.80 1.12 1.20 0.38 0.87 1.19 1.19</p><p>‘CM 2136-2’ 0.38 0.80 1.12 1.18 0.43 0.94 1.19 1.15</p><p>‘CM 3306-32’ 0.42 0.72 1.02 1.09 0.41 0.76 0.97 1.02</p><p>Average of all cultivars 0.39 0.76 1.05 1.13 0.40 0.85 1.09 1.12</p><p>Note: The lack of large changes in leaf water potential during the day between unstressed and stressed crops. Average predawn (as measured at 0600 h) and</p><p>midday (as measured at 1400 h) water potential values were not significantly different between the two watering regimes, indicating the tight stomatal</p><p>control over water losses. The partial closure of stomata under stress (see Table 2 and Figure 3) reduced leaf transpiration rate (see Figure 4), and, hence,</p><p>led to stable leaf water content. This stomatal mechanism is beneficial in preventing severe leaf dehydration and impairment of the photosynthetic process</p><p>as indicated by the rates of net photosynthesis under stress being ca. 80% those in unstressed leaves (see Table 2). Cassava tolerates prolonged water</p><p>shortages via stress avoidance mechanism. When stomatal closure is coupled with rooting system that penetrates into deep wet soil layers (see Figure 6 for</p><p>patterns of water extraction), crop water use efficiency is maximized under drought conditions. These characteristics are beneficial in ecosystems where</p><p>excess rainfall is partially stored in deeper soil layers.</p><p>Table 4. Effect of water stress imposed at different stages of growth on storage root yield and shoot biomass at 12 months after planting,</p><p>and on mean leaf area index (Mean LAI) over the growth cycle for four cassava cultivars grown at Santander de Quilichao, Cauca,</p><p>Colombia in 1991-1992 and 1992-1993. Data are means of two years. Harvests were made 12 months after planting. From El-Sharkawy</p><p>and Cadavid (2002). Permission conveyed through Copyright Clearance Center, Inc</p><p>Cultivar Treatment Treatment Treatment</p><p>Control Early† Mid- Terminal† Control Early Mid- Terminal Control Early Mid- Terminal</p><p>season† Season season</p><p>Dry root yield (t ha-1) Dry shoot biomass (t ha-1) Mean LAI</p><p>‘CM 507-37’ 14.0 11.1 11.3 11.1 6.0 2.7 5.6 5.3 2.3 1.3 1.8 2.3</p><p>‘CM 523-7’ 13.8 12.8 12.1 9.7 5.3 4.2 5.2 4.5 2.3 1.4 1.3 2.0</p><p>‘CMC 40’ 10.0 10.4 12.1 14.6 7.8 3.9 5.7 6.7 1.7 1.1 1.1 1.7</p><p>‘M Col 1684’ 13.6 10.3 12.5 11.5 5.0 2.2 4.0 4.3 1.8 1.1 1.3 1.8</p><p>Average 12.9 11.2 12.9 11.7 6.0 3.3 5.1 5.2 2.0 1.2 1.4 2.0</p><p>LSD (P = 0.05)</p><p>Treatment NS 0.8 0.3</p><p>Treatment x</p><p>Cultivar 2.7 1.4 0.5</p><p>NS, non-significant; P > 0.05; †Early stressed-plants were deprived of water from 2-6 months after planting; Mid-season stressed-plants were deprived of water</p><p>from 4-8; Terminal stressed-plants were deprived of water from 6-12 months. Before imposing water stress by covering the soil with plastic sheets, the</p><p>soil-water to 2-m depth was brought to field capacity by irrigation. During the water stress period, plants depended on stored water only which was about</p><p>200 mm in the 2-m depth. The total extracted water during stress varied from ~150 to 180 mm, depending on cultivar and treatment.</p><p>Notes: (i) the lack of significant difference due to water treatment in root yield across cultivars; (ii) the significant reduction in shoot biomass and Mean LAI</p><p>due to water stress, particularly in early stress; (iii) the significant treatment x cultivar interactions; (iv) the highest (14.6) and lowest (9.7) yields were</p><p>obtained under terminal stress for cv. ‘CMC’ 40 and ‘CM 523-7’, respectively; (v) cultivars ‘CM 507-37’ and ‘M Col 1684’ showed intermediate responses</p><p>to water stress. Because of reductions in shoot biomass, and consequently reductions in total nutrient uptake, in early and mid-season water stress, average</p><p>nutrient-use efficiency (kg dry root per kg total nutrient uptake) was increased by 14 to 40%, depending on water treatment and element (El-Sharkawy et</p><p>al., 1998; El-Sharkawy and Cadavid, 2002; Table 5). Under terminal stress there were smaller increases in nutrient-use efficiency because the peak nutrient</p><p>uptake occurred at 5-6 month after planting and before the start of stress. Early stress seems beneficial in low-fertility soils under bimodal rainfall patterns.</p><p>In this case, cassava should be planted toward the end of the rainy period, pass into a dry period, and then into a second wet period. Even cassava shed most</p><p>of its leaf canopy under prolonged drought, it recovers quickly in subsequent wet conditions forming reasonable canopy with higher leaf photosynthetic</p><p>rates (El-Sharkawy et al. 1992b; El-Sharkawy 1993, 2006a; Cayón et al. 1997).</p><p>Mabrouk A. El-Sharkawy</p><p>86</p><p>Figure 6. Water uptake of ‘M Col 1684’ from different layers of soil at Quilichao, Colombia, as a</p><p>function of time after excluding rainfall (the soil was irrigated to field capacity before being covered</p><p>with white plastic sheets from 22 September 1986 to 5 January 1987). During the first 35 d of stress</p><p>water uptake was 93 mm and at the end of stress the total uptake was 160 mm, i.e. 70-75% of available</p><p>water within 2.0 m depth of soil. Data average of four profiles. From CIAT (1987-1989) Report.</p><p>Also, it is possible that the phenomenon of “hydraulic lift” ﴾i.e. nocturnal uptake of water</p><p>from deeper wet soil layers that is transported and then released from fine roots into dryer top</p><p>soil layers) occurs in cassava since predawn Ψw in water-stressed plants always remained as</p><p>high as in well-watered plants. This might be the case because the majority of fine roots exist</p><p>in the top 0.40 m and a fewer portion of roots penetrate deeper layers (Connor et al., 1981; El-</p><p>Sharkawy and Cock, 1987b; Tscherning et al., 1995) where a substantial water extraction</p><p>occurs (Figure 6). Water uptake from upper layer (0.40 m) continued during long period of</p><p>water deficit with decreasing patterns over time (Figure 6; El-Sharkawy et al., 1992b; de</p><p>Tafur et al., 1997a; El-Sharkawy, 2006a), thus indicating the existence of available water in</p><p>this layer. Another characteristic that might be implicated in cassava tolerance to prolonged</p><p>water stress is the obligate association with vesicular-arbuscular mycorrhizal fungi (VAM)</p><p>(Howeler and Sieverding, 1983; Sieverding and Howeler, 1985). Among 20 cassava cultivars</p><p>Cassava</p><p>87</p><p>growing in large pots outdoors, the percent infected root length under stress varied from ~50</p><p>to ~90%, and these values were highly correlated with total plant root length across cultivars</p><p>(r = 0.955, P < 0.001) (Sieverding et al., 1985). There is some evidence that plant-VAM</p><p>associations may confer tolerance to water stress, particularly in species with low fine root</p><p>density (Hayman, 1980; Nelsen and Safir, 1982; Ellis et al., 1985; Safir, 1985; Augé et al.,</p><p>1987; Khalvati et al., 2005). Compared to cereal crops and tropical forage grasses, cassava</p><p>has a sparse fine root system (Tscherning et al., 1995), and the extensive fungal hyphae-</p><p>network in the soil may increase water absorption capacity of infected roots. For example,</p><p>Khalvati et al. (2005) found that VAM-infected plants suffered less (relative to non-infected</p><p>plants) from water stress in terms of leaf elongation rate, leaf turgor pressure, gs and A. These</p><p>parameters indicate a better plant water status in VAM-infected plants.</p><p>Figure 7. Response of field-grown cassava to prolonged midseason water stress. Cassava plants were</p><p>deprived of water by covering the soil surface with white plastic sheets for three months, commencing</p><p>90 d after planting. Plants recovered from stress (see arrows in A</p><p>and B) under rainfall and</p><p>supplemental irrigation for the rest of the growth cycle. The control plants received normal rainfall plus</p><p>supplemental irrigation. Leaf gas exchange was monitored with a portable infrared gas analyzer</p><p>throughout the stress and recovery periods. A. Leaf photosynthesis during stress and recovery for leaves</p><p>developed under stress. B. Stomatal conductance. C. and D. Photosynthesis and stomatal conductance</p><p>for new leaves developed after stress was terminated. From CIAT, Cassava Physiology Section</p><p>database (1991) Annual Report.</p><p>Mabrouk A. El-Sharkawy</p><p>88</p><p>Figure 8. Leaf gas exchange as a function of time of measurement at Riohacha (semiarid) and Santo</p><p>Tomas (seasonally dry). Data are averages of 14 cultivars. RH: atmospheric relative humidity. From</p><p>CIAT (1993).</p><p>A fourth mechanism underlying tolerance to drought is the ability of cassava to</p><p>compensate partly for previous losses in dry matter production, due to water deficit, by an</p><p>increase in leaf canopy area (El-Sharkawy and Cock, 1987b; El-Sharkawy et al., 1992b) and</p><p>by higher A in the newly developed leaves after recovery, as compared to the unstressed</p><p>plants (Figure 7) (El-Sharkawy, 1993, Cayón et al., 1997; de Tafur et al., 1997a; El-</p><p>Sharkawy, 2006a). Higher A in new leaves of previously stressed cassava was associated with</p><p>higher leaf conductance, higher nutrient contents, as well as with stronger sinks for</p><p>carbohydrate in storage roots (Cayón et al., 1997).</p><p>Not only can cassava tolerate long periods of soil water deficits aided with the above-</p><p>mentioned inherent mechanisms, but it can also react to changes in atmospheric humidity</p><p>(Figure 8) (Connor and Palta, 1981; El-Sharkawy and Cock, 1984, 1986, 1990; El-Sharkawy</p><p>et al., 1984, 1985, 1989; Cock et al., 1985; Berg et al., 1986; El-Sharkawy, 1990, 1993, 2004,</p><p>2006a; Oguntunde, 2005; Oguntunde and Alatise, 2007). Cassava leaf stomata are sensitive to</p><p>air humidity, irrespective of soil water content; they close rapidly in dry air when evaporation</p><p>is high under field conditions, which may be translated into high leaf Ψw. This mechanism</p><p>Cassava</p><p>89</p><p>enables cassava to maximize its WUE during periods of prolonged drought. When air</p><p>humidity is high (e.g. early in the morning and during rainy periods), the stomata remain</p><p>open. Thus, in a humid atmosphere and in the presence of soil water deficits, cassava leaves</p><p>remain photosynthetically active and the crop can produce well; for example, in the Pacific</p><p>coast of Ecuador, cassava produces 8 to 12 t ha-1 of fresh roots with only 400 mm of rainfall</p><p>in 3-4 months. In that region, the intensity of solar radiation is low because of cloudy skies</p><p>and, hence, evaporation is low. A similar situation occurs in the Pacific coast of Peru where</p><p>rainfall is very low but there is an intense fine mist or fog that persists for hours, allowing</p><p>stomata to remain partly open and the leaf to actively fix CO2 at a lower E. Thus, WUE at the</p><p>leaf level (CO2 uptake per H2O loss) and at the crop level for the whole growing cycle (dry</p><p>matter produced per total water loss) are maximized in this case. Cock et al. (1985) found that</p><p>increasing air humidity by fine misting from 1000 h to 1500 h, in a large cassava field</p><p>experimental plot that was kept wet via irrigation and protected from wind drift by hedge</p><p>rows of tall elephant grass at the CIAT Experiment Station, Palmira, Colombia, resulted in</p><p>both higher A and higher root yields than in the adjacent unmisted plot that was equally</p><p>irrigated. Moreover, leaf A was significantly and positively correlated with air humidity,</p><p>indicating stomatal reactions to air humidity even in a wet soil (Figure 9).</p><p>Figure 9. The apparent photosynthetic rate of field-grown cassava as a function of atmospheric relative</p><p>humidity. Misted (solid symbols) and non-misted (open symbols) ‘M Col 1684’ cassava plants. Soil</p><p>was wet in both treatments. From Cock et al. (1985) with permission of Crop Science.</p><p>Coupled with stomatal sensitivity to air humidity is the strong leaf heliotropic response</p><p>that allows leaves to track solar radiation early in the morning and late afternoon when the</p><p>leaf-to-air water vapor deficit (VPD) is low. At midday when solar elevation is high and VPD</p><p>is greatest, cassava leaves bend downward (i.e. leaf drooping movement) irrespective of SWC</p><p>Mabrouk A. El-Sharkawy</p><p>90</p><p>and leaf turgor pressure (El-Sharkawy and Cock, 1984; Berg et al., 1986). The net result of</p><p>these two leaf movements is to maximize light interception and total canopy photosynthesis</p><p>when WUE is greatest, and to minimize light interception when WUE is least.</p><p>In the present trial, the four months during which soil water stress was imposed coincided</p><p>with a rainfall peak (total rainfall in April and May 1988 at Quilichao was 400 mm). During</p><p>April and May 1988, the last two months of the stress period, A of the stressed plants was</p><p>60% to 70% of those in the control plants (Figure 3). This remarkable photosynthetic activity</p><p>of the stressed cassava can be attributed partly to the favorable effects of high humidity which</p><p>kept the stomata partly open (Figure 4). It may be concluded that cassava is extremely</p><p>tolerant (or resistant) to prolonged drought because of multiple-inherent morphological,</p><p>structural and physiological plant traits that allow the crop to obviate the negative effects of</p><p>severe water stress.</p><p>Response to Prolonged Drought Imposed at Different Stages of Plant Growth</p><p>Based on the above findings on response of cassava to early- and mid-season stress it was</p><p>warranted, therefore, to simulate naturally occurring water deficits at different stages of plant</p><p>growth. The same trends, as discussed above, in responses to extended water deficits imposed</p><p>at early (2-6 months after planting), mid-season (4-8 months after planting) and terminal (6-</p><p>12 months after planting) growth stages were observed in a 3-yr field trial with four</p><p>contrasting cultivars that differed in their vigor (CIAT, 1992, 1993; Caicédo, 1993; El-</p><p>Sharkawy et al., 1998; El-Sharkawy and Cadavid, 2002; El-Sharkawy, 2006a). Across</p><p>cultivars there were no significant differences in root yield among water regimes, but there</p><p>were significant differences among cultivars indicating genotypic x treatment interactions (P</p><p>< 0.01) (Table 4). Similar responses were observed in the Sudan Savanna zone of Nigeria</p><p>using variation in the soil-water table as a variable for water availability (Okogbenin et al.,</p><p>2003). These findings support the sound breeding strategy for developing cultivars for</p><p>specific ecozones (Hershey and Jennings, 1992; El-Sharkawy, 1993; Iglesias et al., 1995;</p><p>Jennings and Iglesias, 2002). Moreover, compared to the control, all water deficit treatments</p><p>significantly reduced P, K, Ca and Mg contents in shoot biomass at final harvest that led to a</p><p>lower uptake per land area (El-Sharkawy et al., 1998; El-Sharkawy and Cadavid, 2002). This</p><p>trend in nutrient uptake had resulted in higher nutrient-use efficiency, in terms of storage root</p><p>production, particularly in early- and mid-season water-stressed crops (El-Sharkawy et al.,</p><p>1998; El-Sharkawy and Cadavid, 2002; Table 5). On one hand, the lack of change in N-use</p><p>efficiency in the mid-season stress (see Table 5) was mainly attributed to the smaller</p><p>reduction in shoot biomass where most plant-N is located, and, consequently, to the smaller</p><p>reduction in N content (El-Sharkawy and Cadavid, 2002; see Table 4 for biomass and Table 5</p><p>for N content). On the other hand, the smaller N-use efficiency in terminal stress was due to</p><p>the larger N content in storage roots (see Table 5). As cassava has very low protein content in</p><p>storage roots (< 2 % in peeled dry root; Yeoh and Truong, 1996), the apparent increase in</p><p>storage root N under terminal stress might lead to a higher protein.</p><p>Because of its higher root production in water-stressed crops, compared to the control, cv.</p><p>‘CMC 40’ had the highest nutrient-use</p><p>efficiency for all nutrient elements, indicating its</p><p>utility as a genetic source for breeding and selection of new cultivars adaptable to both water</p><p>stress and low-fertility soils. Maximizing root production per unit nutrient extracted under</p><p>Cassava</p><p>91</p><p>stressful environment is of paramount importance in marginal low-fertility soils as well as in</p><p>fertilized cropping systems. It is noteworthy that ‘CMC 40’, compared to other cultivars, had</p><p>the highest photosynthetic enzyme activities in extracts of upper canopy leaves (8.2 mmol g-1</p><p>Chl min-1 for Rubisco; and 3.1 mmol g-1 Chl min-1 for PEPC) (CIAT, 1992; Lopez et al.,</p><p>1993; El-Sharkawy and Cadavid, 2002; El-Sharkawy and de Tafur, 2007). These high</p><p>enzymatic activities under field conditions might be advantageous for cassava productivity as</p><p>well as its tolerance to drought (El-Sharkawy, 2004; El-Sharkawy et al., 2008; Table 6).</p><p>Table 5. Effect of water stress on nutrient-use efficiency. Data are means of four</p><p>cultivars in two years. Note: the lack of change in N-use efficiency in mid-season stress</p><p>was mainly due to the smaller reduction in shoot biomass (see Table 4) and,</p><p>consequently, the smaller reduction in shoot N concentration (shoot N concentration</p><p>was: 76, 41, 67, 64 kg ha-1 for the control, early stress, mid-season stress and terminal</p><p>stress, respectively). The smaller N-use efficiency in terminal stress was attributed to the</p><p>larger N concentration in storage roots (root N concentration was: 35, 40, 36, 47 kg ha-1</p><p>for the control, early stress, mid-season stress and terminal stress, respectively). From</p><p>El-Sharkawy and Cadavid (2002). Permission conveyed through Copyright Clearance</p><p>Center, Inc</p><p>Treatment Roots (kg DW kg-1 total nutrient content)</p><p>N P K Ca Mg</p><p>Control 120 660 110 300 440</p><p>Early stress 150 940 150 360 650</p><p>Mid-season stress 120 840 140 330 530</p><p>Terminal stress 110 690 120 300 520</p><p>LSD 5% 12 70 9 50 65</p><p>Plant ecophysiologists have proposed a sort of “classification/ terminology” scheme</p><p>based on mechanisms underlying plant adaptation to water deficits (for more information see,</p><p>for example, Levitt 1980; Turner 1986; Ludlow and Muchow, 1990). According to Turner</p><p>(1986), plants that are able to endure long periods of water shortages while maintaining a high</p><p>tissue Ψw are called drought tolerant. Cassava may fit among these types of plants.</p><p>Nevertheless, Alves (2002), working with indoor-grown plants, found no significant</p><p>accumulation of solutes and osmolytes in mature cassava leaves, and, hence, no occurrence of</p><p>osmotic adjustment. This finding further confirms that cassava stomatal control over plant</p><p>water relations is the predominant defense mechanism protecting the leaf from severe</p><p>dehydration, and, consequently, it can be considered a stress avoidance mechanism (El-</p><p>Sharkawy, 2006a). Moreover, the remarkable stomatal control over water loss has important</p><p>implications for breeding strategy of cassava cultivars adapted to different environments. For</p><p>example, in humid and wet areas such as the Amazonia and other hot humid tropical</p><p>rainforests, less sensitive cultivars to changes in VPD are favored as maximizing productivity</p><p>overrides optimizing WUE in this case, whereas in seasonally dry or semiarid areas with</p><p>prolonged drought coupled with much higher evaporative demands sensitive cultivars are</p><p>beneficial in order to optimize WUE.</p><p>Mabrouk A. El-Sharkawy</p><p>92</p><p>Table 6. Correlation coefficients and regression equations for various plant trait</p><p>combinations in 18 cultivars selected from the preliminary-screened 127 in Patia,</p><p>Cauca, Colombia, 1987-1988. Leaf photosynthetic characteristics were determined in</p><p>upper canopy leaves from 5-8 month-old-plants. Leaf nitrogen content and PEP</p><p>carboxylase activity were determined in upper canopy leaves from independent leaf</p><p>samples from 5-month-old-plants. Measurements were made during dry period. n = 18.</p><p>From El-Sharkawy et al. (2008). Permission conveyed through Copyright Clearance</p><p>Center, Inc</p><p>Trait combination Correlation coefficient (r) Regression equation (y = a + bx)</p><p>X y</p><p>A Yield 0.500* Yield= 0.178+ 0.047 A</p><p>PNUE Yield 0.481* Yield= 0.605 + 0.062 PNUE</p><p>PEPC Yield 0.547* Yield= 0.804 + 0.057 PEPC</p><p>gm Yield 0.479* Yield= -0.066 + 0.014 gm</p><p>PEPC A 0.597** A = 18.43 + 0.69 PEPC</p><p>PEPC gm 0.532* gm = 83.5 + 2.0 PEPC</p><p>PEPC PNUE 0.698** PNUE= 6.42 + 0.58 PEPC</p><p>*, ** indicate level of significance at P = 0.05 and 0.01, respectively.</p><p>A, net leaf photosynthetic rate (μmol CO2 m-2 s-1); PNUE, photosynthetic nitrogen-use efficiency [mmol</p><p>CO2 kg-1 (total leaf nitrogen) s-1]; PEPC, phosphoenolpyruvate carboxylase activity (μmol kg-1 FM</p><p>s-1); gm, mesophyll conductance to CO2 diffusion (mmol m-2 s-1); Yield, dry root yield (kg m-2).</p><p>Values of cultivars (means), and ranges: A (25.1), 21-30.6; PNUE (12.1), 9.4-16.2; PEPC activity (9.7),</p><p>6.3-14.0; gm (103), 93-126; Yield (1.36), 1.00-1.83. In these trials, the average PEPC activity in</p><p>cassava was 17% of activity in the C4 grain sorghum grown on the same plot.</p><p>Note: The significant correlations between PEPC activity and photosynthetic characteristics and yield</p><p>of cassava point to the importance of the enzyme as a desirable selectable trait for cultivar</p><p>improvement, particularly under stressful environments.</p><p>BREEDING FOR DROUGHT TOLERANT CASSAVA IN SEASONALLY DRY</p><p>AND SEMI-ARID ENVIRONMENTS IN COLOMBIA AND BRAZIL</p><p>The plan traits and mechanisms discussed above that underlie cassava tolerance to</p><p>prolonged drought have further implications for the possible expansion of adaptable cassava</p><p>cultivars into marginal lands and under adverse climatic conditions. As a potential food and</p><p>feed crop for the tropical and subtropical regions most likely affected by global climate</p><p>changes, cassava will probably become an important food-security source in developing</p><p>countries where there are severe food shortages (Rosenzweig and Parry, 1994;</p><p>Kamukondiwa, 1996; El-Sharkawy, 2005; IPCC, 2006). Rosenzweig and Parry (1994)</p><p>pointed out that cereal crop production in the tropics and subtropics will possibly decrease in</p><p>the near future because of global climate changes, hence, food shortages would be further</p><p>aggravated in these regions.</p><p>Cassava</p><p>93</p><p>Selection for Drought Tolerance in Cassava For Seasonally Dry and</p><p>Semiarid Environments in Colombia</p><p>The physiological research, as discussed above, laid the foundation for improving the</p><p>cassava genetic base, and for selection for drought tolerance in seasonally dry and semiarid</p><p>environments where a significant portion of cassava production occurs (El-Sharkawy, 1993;</p><p>Iglesias et al., 1995). A large group of cassava from the core germplasm collection was</p><p>screened for leaf photosynthesis and productivity in seasonally dry and semiarid</p><p>environments in Colombia.</p><p>Evaluation of core germplasm for productivity and photosynthesis in seasonally dry</p><p>environments at the southwest Andean mountains of Colombia: In the 1986-1987 growing</p><p>season, 127 CIAT cassava accessions, including cultivars, land races and breeding lines were</p><p>screened on a private farm in the Patia Valley (600 m a.s.l., 2o09´N, 77o04’W, mean annual</p><p>temperature 28oC with little seasonal variation, average atmospheric humidity about 70%),</p><p>Colombia. The soils in Patia Valley are heavy clay, and the farm was under continuous</p><p>pasture grasses for the last 25 yr. The trial was planted at a population density of 15,625 plant</p><p>ha-1 on 23 October 1986, with adequate fertilization. The site received about 700 mm of rain</p><p>in 309 d, but from December 1986 to April 1987, the rainfall was much less than the potential</p><p>evaporation which was greater than 5 mm d-1. The Patia Valley, lying between the central and</p><p>western Andes mountains, is characterized by two wet periods (October-December and</p><p>March-June), and with high solar radiation of about 22 MJ m-2 d-1. The 1986-1987 season was</p><p>particularly dry, with</p><p>no rainfall recorded from June to August. The trial was harvested on 26</p><p>to 27 August 1987.</p><p>Measurements of single-leaf gas exchanges were made with a portable infrared gas</p><p>analyzer using central lobes of upper canopy leaves on several occasions between February</p><p>and June 1987. At this stage of crop growth, LAI was near its peak, and storage root bulking</p><p>rate was greatest, and, hence, both carbon source capacity and root-sink demand were near</p><p>optimal. Measurements were always made from 0900 to 1300 h when the solar irradiance</p><p>exceeded 1000 µmol m-2 s-1 of PAR. Leaf Ψw, determined on lobes from the same leaves used</p><p>for gas exchange, ranged from -1.0 to -1.5 MPa, across varieties and measurement dates.</p><p>Contents of N, P, and K were also determined on the same measured leaves (El-Sharkawy et</p><p>al., 1990).</p><p>Across all accessions, both fresh total plant biomass and dried root yield were highly</p><p>significantly and positively correlated with average leaf A, and the correlation was higher in</p><p>the high and medium top weight varieties than in the low top ones. These results indicate that,</p><p>on the one hand, at high level of light interception (i.e. near optimum LAI in high and</p><p>medium top weight) there was a direct relationship between productivity and leaf A. On the</p><p>other hand, at lower light interception because of lower than optimal LAI in the low top</p><p>genotypes, the relation is weaker and light interception appears to be the predominant factor</p><p>in determining productivity. Thus, when both canopy light interception and root-sink demand</p><p>for carbohydrates are not limiting, productivity correlates well with leaf A, as measured in the</p><p>field (El-Sharkawy et al., 1989, 1990; El-Sharkawy and Cock, 1990).</p><p>Sixteen clones were selected from the many screened accessions on the basis of their</p><p>high-yield performance, and were planted on 13 April 1988, in another adjacent private farm</p><p>in the Patia Valley, and at a population density of 10,000 plants ha-1. A split-block design</p><p>Mabrouk A. El-Sharkawy</p><p>94</p><p>with four replications was used to allow for two fertilization treatments: (i) without</p><p>fertilization; and (ii) with 50, 100 and 100 kg NPK ha-1. The crop received about 950 mm of</p><p>rain during the growing cycle of 308 d, with 560 mm out of the total rainfall occurring in</p><p>October and November 1988, which resulted in a significant amount of water runoff. On 14-</p><p>16 February 1989, plants were harvested to determine biomass and root yield weight.</p><p>Measurements of single-leaf gas exchanges were made only once per day on 29 August to 7</p><p>September 1988. Across all blocks and fertilizer treatments, 35 fully expanded upper-canopy</p><p>leaves were measured per cultivar. All measurements were made from 0800 h to 1300 h with</p><p>solar irradiance exceeding 1000 µmol m-2 s-1 of PAR, and normal air with 320 ± 10 µmol</p><p>CO2 mol-1.</p><p>Since no significant fertilizer effects were observed in root yield and gas exchange rates,</p><p>data were pooled. Average root yields were higher than those in the 1986-1987 preliminary</p><p>screening trial, and this was mainly attributed to the higher rainfall in 1988-1989, as well as to</p><p>the smaller group of selected high-yielding clones. The mean dry root yield among the 16</p><p>cultivars ranged from 15 to 27 t ha-1, indicating the high yield potential in cassava when</p><p>grown in near optimal environments. In this trial with nearly 9000 m2 land including borders,</p><p>the overall average dry root yield harvested from the whole area exceeded 20 t ha-1.</p><p>Despite differences in rainfall between the two growing seasons, leaf A measured in</p><p>1986-1987 season was highly significantly and positively correlated with the dry root-yield of</p><p>the 1988-1989 season (Figure 10). Furthermore, average leaf A, as measured only once in the</p><p>1988-1989 season, was significantly correlated with rates measured over a more extended</p><p>period of time in the 1986-1987 season (Figure 11).</p><p>Figure 10. Relationship between the 1988/1989 dry root yield and the single-leaf photosynthesis</p><p>measured in the 1986/1987 season. Data of yield are averages of eight of replications, 16 cultivars.</p><p>From El-Sharkawy et al. (1990) with permission of Elsevier, Inc.</p><p>Cassava</p><p>95</p><p>Figure 11. Relationship between the 1988/1989 leaf photosynthesis measured once with the open-end</p><p>LCA-2 apparatus, at 4 months after planting and the 1986/1987 rates measured with the LI-6000</p><p>closed-circuit apparatus on three occasions at 4-6 months after planting. From El-Sharkawy et al.</p><p>(1990) with permission of Elsevier, Inc.</p><p>Figure 12. Relationship between dry root yield and leaf photosynthesis of the 1988/1989 season. Data</p><p>of yield are averages of eight replications, 16 cultivars. From El-Sharkawy et al. (1990) with permission</p><p>of Elsevier, Inc.</p><p>Mabrouk A. El-Sharkawy</p><p>96</p><p>The dry root yield and the average leaf A of the 1988-1989 season crop were also</p><p>significantly correlated (Figure 12). These data clearly demonstrate the consistent relation</p><p>over years between upper canopy single-leaf photosynthesis, as measured in the field, and</p><p>productivity in cassava.</p><p>The relation between leaf A and productivity was mainly due to nonstomatal factors (i.e.</p><p>due to biochemical and/or anatomical leaf characteristics), as demonstrated by the negative</p><p>significant correlation between yield and intercellular CO2 concentration (Ci) (El-Sharkawy et</p><p>al., 1990). This conclusion is further substantiated by the significant positive correlation</p><p>between yield and photosynthetic N-use efficiency (PNUE = CO2 uptake per unit total leaf</p><p>nitrogen, Figure 13). Leaf anatomical characteristics that may affect the amount and</p><p>distribution of photosynthetic machinery can play a significant role in leaf photosynthesis.</p><p>But since yield is significantly correlated with PNUE, it appears, therefore, that biochemical</p><p>factors affecting photosynthesis, such as activities of photosynthetic enzymes, are more</p><p>important in this case. Leaf A of various cassava varieties subjected to water stress in the field</p><p>was significantly and positively correlated with the activity of the C4 enzyme PEPC in</p><p>extracts of the same measured leaves (El-Sharkawy, 2004). Table 6 presents correlation</p><p>coefficients and regressions between yield, photosynthetic characteristics, and PEPC activity</p><p>in 18 varieties selected from the preliminary trial in Patia. There were significant correlations</p><p>between yield, photosynthetic characteristics and PEPC activity. The PEPC activity was</p><p>highly significantly correlated with A and PNUE (Table 6). Moreover, PEPC activity in</p><p>Figure 13. Relationship between dry root yield and leaf nitrogen use efficiency in field-grown cassava.</p><p>Leaf nitrogen use efficiency values were calculated from leaf CO2 exchange measurements and total</p><p>leaf nitrogen concentrations. Data for 40 cultivars with high shoot weight. From El-Sharkawy (2004).</p><p>Permission conveyed through Copyright Clearance Center, Inc.</p><p>Cassava</p><p>97</p><p>cassava was much greater than that observed in typical C3 plants and about 10-30% of the</p><p>activity in typical C4 species such as maize and sorghum (El-Sharkawy et al., 1989, 2008; El-</p><p>Sharkawy and Cock 1990; El-Sharkawy, 2004, 2006a). Also, it is possible that differences in</p><p>leaf A within cassava germplasm could be due partly to differences in characteristics of the C3</p><p>enzyme, Rubisco. Paul and Yeoh (1987, 1988) reported wide variation in kinetic properties of</p><p>cassava Rubisco. Values of Km (CO2) for 16 cassava varieties ranged from 7.8 to 14.0 µM</p><p>CO2, while Km (RuBP) values ranged from 7.5 to 24.8 µM RuBP. Wide variation was also</p><p>found in activities of Rubisco among cassava genotypes (López et al., 1993; El-Sharkawy,</p><p>2004, 2006a). Thus, selection for high photosynthetic rates and high enzyme activity would</p><p>be beneficial for breeding improved cassava varieties, particularly under drought conditions.</p><p>Evaluation of core germplasm in both seasonally dry and semiarid environments in</p><p>northern coast of Colombia: Two field trials</p><p>drought conditions. However, studies on the effects of drought on crop</p><p>performance are often complicated, firstly due to the complex nature of drought stress in the</p><p>field, and secondly because crop yield may be affected more directly by a smaller leaf area</p><p>rather than by the decreased photosynthetic rate per unit leaf area during and following</p><p>drought events.</p><p>Long diurnal periods with air temperatures above 35oC are relatively common in tropical</p><p>areas. High air temperatures may quickly increase the leaf-to-air temperature difference to</p><p>values above 5 to 10oC or more, as shown for tea. One of the major difficulties in interpreting</p><p>the response of physiological processes such as photosynthesis to temperature, particularly in</p><p>the field, is that temperature increase is associated with a rise in the atmospheric vapor</p><p>pressure deficit. Therefore, decreases in photosynthetic rates could be due to either increases</p><p>in temperature per se or increases in the vapor pressure deficit leading to stomatal closure, or</p><p>both. However, in contrast to temperate species (see, for example, Salisbury and Ross, 1992),</p><p>there seems to be a broad adequate temperature range (20-35ºC, or even above) for</p><p>photosynthesis, nearly corresponding to the normal temperature fluctuations frequently found</p><p>in the hot environments in which tropical tree crops are generally grown (DaMatta, 2003). For</p><p>example, by growing cassava in a hot environment, El-Sharkawy and Cock (1990)</p><p>demonstrated that maximum values for the net photosynthetic rate of around 30 to 36 μmol</p><p>m-2 s-1 were common, with leaf temperature in the range 32 to 37oC. They also pointed out</p><p>that failure to adequately control air humidity and irradiance was responsible for the findings</p><p>of several earlier reports showing lower cassava photosynthesis and lower and narrower</p><p>optimum temperatures of 25 to 28oC for maximum photosynthetic rates.</p><p>Fábio M. DaMatta</p><p>4</p><p>Manipulation of microclimates for increasing the efficiency with which resources are</p><p>used in agriculture has received renewed attention in recent years. In agroforestry and inter-</p><p>cropping systems, taller plant canopies may alter not only the radiation, but also air humidity</p><p>and temperature around understory crops. The seedlings of many tropical tree crops grow</p><p>better under shaded conditions than in full sunlight (e.g., cocoa, tea), perhaps because they are</p><p>subjected to photoinhibition, and/or have large root resistances to water uptake resulting in</p><p>early stomatal closure. During the juvenile phase of tree crops, inter-cropping with fast-</p><p>growing tree crops such as cassava, papaya and banana is often successfully used. This allows</p><p>not only improved light capture and biomass production per unit land area but also improved</p><p>growth as a result of a more favorable water status. In fact, it may be suggested that shading,</p><p>provided it is not excessive, may be advantageous for tree crop cultivation in the tropics,</p><p>considering that (i) photosynthesis in several tropical tree crops is light-saturated below full</p><p>sunlight; (ii) in the tropics during most of the year incoming radiation is high and may lead to</p><p>photoinhibitory damage, particularly when associated with water shortage; and (iii) improved</p><p>microclimates lead to a buffering of air humidity and soil moisture availability, thereby</p><p>allowing longer maintenance of leaf gas exchange. Other reasons for maintaining shade trees</p><p>with perennial crop plantations include the income provided by their fruit and/or timber (or</p><p>latex if rubber is the dominant species), increasing awareness of the environmental costs</p><p>associated with high-input monocrops, and biodiversity maintenance. Indeed, a growing body</p><p>of evidence suggests that when correctly managed, inter-cropping and agroforestry schemes</p><p>will become a promising alternative for sustainability in tropical agriculture, as highlighted</p><p>here for crops such as cocoa, coffee, rubber, and tea.</p><p>FUTURE SCOPE</p><p>There is an increasing trend for expanding tropical agriculture towards marginal and</p><p>degraded lands where water shortage and unfavorable temperatures already constitute major</p><p>constraints to crop yield. The scientific community has long been aware of the impact of the</p><p>environment on plant productivity, and this aspect of plant biology has recently become a</p><p>greater political and public concern in the wake of discussions surrounding global climate</p><p>change (Chapple and Campbell, 2007). Large areas of valuable irrigated land are facing crop</p><p>conversion problems because they either are allotted to less valuable annual crops or have</p><p>critical salinization problems (roughly one-fourth of the irrigated land world-wide; Janssens</p><p>and Subramanim, 2000). Considerable areas with sufficient water now will experience some</p><p>degree of water shortage in the near future, e.g., India and parts of China (Wallace, 2000).</p><p>The use of appropriate perennial crops in combination with adequate irrigation to exploit</p><p>saline lands may be successful where annuals would normally fail. In addition, perennial</p><p>crops may help buffer farmer's production against year-to-year oscillations in yield from</p><p>rainfed annual crops. In effect, in the latter half of the last century, most particularly in the</p><p>last decade, the proportion of annual to perennial crops evolved more in favor of the latter.</p><p>There is also an expectation that the proportion of perennial crops to annual crops will</p><p>continue to increase during this century (Janssens and Subramaniam, 2000). Most of this</p><p>increase is in tropical and subtropical tree crops. It is unnecessary to point out that there are</p><p>Introduction</p><p>5</p><p>uncountable tropical species with potential agricultural use that have not yet been</p><p>domesticated.</p><p>As occurs with most tropical plant species, the gaps in our knowledge of the</p><p>ecophysiology of tropical tree crops are incommensurable, though significant advances have</p><p>occurred in recent years. The bulk of research has slowly been shifted from more</p><p>observational studies of plant growth and developmental responses to physiological</p><p>processes, as can be seen in the current chapters dealing with banana, citrus, coffee and</p><p>mango. Unfortunately, however, physiological research on tropical tree crops has been</p><p>restricted to a few laboratories throughout tropical/subtropical countries where those crops are</p><p>chiefly grown. To date, significant fundamental research has been conducted using potted</p><p>plants without the appropriate calibration in the field, which can lead to a waste of time and</p><p>resources since in most cases results cannot be extrapolated or simulated by crop modeling to</p><p>describe what may occur in natural environments (El-Sharkawy, 2006; Long et al., 2006).</p><p>Even under field conditions, much emphasis has been focused at the leaf level without</p><p>advancing substantially towards the canopy level. Furthermore, part of the available</p><p>information from field conditions is based on empirical experimentation, rather than</p><p>scientifically-based work, with predominantly observational results and no mechanistic or</p><p>functional links. With a few exceptions, the use of isotope techniques, fundamental</p><p>biochemical and molecular studies, multiscale analyses, and crop simulation models have not</p><p>yet been the major goals of basic and applied research in tropical tree crops. Based on this, a</p><p>deep understanding of the physiology of currently cultivated tropical trees and its impact on</p><p>subsistence and commercial agriculture is a challenge to be handled in the near future.</p><p>Hopefully, this book will not only highlight some recent advances in the ecophysiology</p><p>of tropical tree crops, but also may serve as a stimulus for further efforts in this important and</p><p>challenging field of research. As yet we are waiting for the new tools in genetics,</p><p>biochemistry and molecular biology that are just beginning to be explored in major crops such</p><p>as coffee and citrus to be expanded to other tropical tree crops. It must be emphasized,</p><p>however, that if significant</p><p>were conducted during the 1992-1993 season in</p><p>two locations at the northern coast of Colombia using two groups of cassava clones selected</p><p>from the CIAT core germplasm. One trial was conducted on a private farm at Santo Tomas</p><p>(14 m a.s.l., 10o57΄N, 74o 47΄W), Atlantic Department. At this site the mean annual rainfall of</p><p>830 mm is 50% of the mean annual pan evaporation of 1650 mm, with a rainy period from</p><p>May to November and a dry period from December to April. The soil at the site is sandy (></p><p>80% sand) with low water holding capacity, very low in organic matter and low in nutrients.</p><p>The second trial was conducted at a site (4 m a.s.l., 11o32΄N, 72o56΄W) near Riohacha,</p><p>Guajira Department. At that site the mean annual rainfall of about 560 mm is 25% of the</p><p>mean annual pan evaporation of 2300 mm. The rainfall distribution pattern in this region is</p><p>characterized by a short rainy period from September to November, a dry period from</p><p>December to April, and a second low-rainfall period from May to August. The soil in that site</p><p>is sandy (> 80% sand) with low water holding capacity, very low in organic matter and</p><p>nutrients. In both trials, no chemical fertilizer was applied.</p><p>Under the above-mentioned stressful environments, average oven-dried root yield was</p><p>6.7 t ha-1 at the seasonally dry location (yield ranged among cultivars from 5.8 to 7.6 t ha-1),</p><p>whereas at the semiarid location overall average yield was 2.3 t ha-1 (yield ranged among</p><p>cultivars from 0.4 to 3.3 t ha-1). These levels of productivity, without fertilization and with</p><p>severe prolonged drought, illustrate again the high adaptability of cassava to adverse</p><p>atmospheric and edaphic conditions. Moreover, the crop not only survived but also produced</p><p>reasonably well, where other major staple food crops like tropical cereals would not be able to</p><p>compete with cassava. The most drought-tolerant tropical cereals such as grain sorghums and</p><p>millets (Blum and Sullivan, 1986) perhaps would fail to produce under the semiarid</p><p>conditions experienced in these trials. Nevertheless, because of the severe shortage of rainfall</p><p>in the semiarid environment, root dry matter content was lower (less than 30%) than in</p><p>seasonally dry environments. In practice, however, such as in northeastern Brazil with mean</p><p>annual rainfall less than 700 mm, the crop is allowed to go into a second wet cycle that leads</p><p>to higher yields as well as higher root dry matter content.</p><p>Measurements of leaf gas exchanges were made during several days from February to</p><p>March, 1993. All measurements were made on upper canopy leaves between 0800 h and 1200</p><p>h local time with a solar irradiance higher than 1000 µmol m-2 s-1. Measurements were taken</p><p>during the dry period four to five months after planting at air temperatures within the leaf</p><p>cuvette ranging from 29 to 37oC, depending on time and date of measurements. This range of</p><p>temperatures is near the optimum for photosynthesis in cassava as measured under controlled</p><p>laboratory conditions (El-Sharkawy and Cock, 1990; El-Sharkawy et al., 1992a). Overall</p><p>Mabrouk A. El-Sharkawy</p><p>98</p><p>average A across cultivars was much higher at the seasonally dry site than at the semiarid site,</p><p>with the highest rates observed early in the morning and the lowest at midday (Figure 8) (de</p><p>Tafur et al., 1997b). Leaf gs showed the same trend, indicating the striking effect of air</p><p>humidity on stomatal opening as previously observed under controlled laboratory conditions</p><p>(El-Sharkawy and Cock, 1984, 1986; El-Sharkawy et al., 1984, 1985). These photosynthetic</p><p>rates are much lower than the maximum rates (> 40 µmol CO2 m-2 s-1) that are normally</p><p>observed in field-grown cassava in wet soils and with high atmospheric humidity (El-</p><p>Sharkawy et al., 1992a, 1993). However, compared with other field crops, cassava is more</p><p>photosynthetically active under severe prolonged drought, an advantage that underlies its</p><p>remarkable productivity and ability to endure harsh environments. Thus, it is beneficial to</p><p>select for higher photosynthetic capacity, combined with other desirable plant traits such as</p><p>longer leaf life (better leaf retention and duration; Lenis et al., 2006) and deeper and extensive</p><p>fine root systems in order to enhance growth and yield in dry areas.</p><p>In both environments, dry root yield was highly significantly and positively correlated</p><p>with average leaf A (Figure 14, r2 = 0.76, P < 0.01) (CIAT, 1995; de Tafur et al., 1997b).</p><p>Moreover, dry root yield was highly significantly and negatively correlated with Ci (Figure</p><p>15), indicating that the relation is due mainly to nonstomatal factors controlling leaf</p><p>photosynthesis. These results corroborate other findings in humid and sub-humid/seasonally</p><p>dry environments, as discussed above (El-Sharkawy et al., 1990, 1993; Pellet and El-</p><p>Sharkawy, 1993; El-Sharkawy, 2006a). The results also point to the importance of utilizing</p><p>genetic variations in photosynthetic enzyme characteristics as selection criteria in cassava</p><p>breeding, particularly for improved genotypes targeted for dry environments. The C4 PEPC,</p><p>in particular, plays a significant role in cassava photosynthesis, when the numerous abaxial</p><p>stomata close in hot-dry environments. Under this situation, PEPC recycles respiratory CO2,</p><p>and, hence, dissipates excess solar energy and obviates photoinhibition of the photosynthetic</p><p>process.</p><p>Breeding for drought tolerance in cassava under the semiarid conditions of northeastern</p><p>Brazil: Besides being, for millennia, the main geographical site for the origin of cassava, the</p><p>center for its genetic diversity and for its domestication (Allem, 2002), Brazil is the largest</p><p>cassava producer in Latin America. According to FAOSTAT (2008), the 2007 area harvested</p><p>under cassava in Brazil was about 1.94 million ha, about 24% more than that in 1999 and the</p><p>total fresh root production was 27.3 million tons (12.0% of world 2007 estimated production</p><p>of about 228 million tons). The estimate of root yield across the country was 14.0 t ha-1 for</p><p>2007, slightly higher than that in 1999 (about 13.4 t ha-1). Almost 50% of the total Brazilian</p><p>cassava production comes from the more marginal regions of the semiarid northeastern,</p><p>strengthening the importance of improving the genetic base of cassava, and for breeding new</p><p>cultivars more adapted to the severe water stress conditions prevailing in that region. This</p><p>objective was further strengthened by the knowledge of cassava’s inherent potential for</p><p>drought tolerance and the newly acquired basic physiological information and insights about</p><p>the mechanisms underpinning such tolerance.</p><p>Cassava</p><p>99</p><p>Figure 14. Relationships between root yield and leaf photosynthesis of several cassava clones grown in</p><p>seasonally dry (Santo Tomás, Atlántico) and semiarid (Riohacha, Guajira) environments. From CIAT</p><p>(1995) Report.</p><p>Figure 15. Relationship between dry root yield and intercellular CO2 concentration (Ci) for two groups</p><p>of cassava cultivars grown under rain-fed conditions at Riohacha (semi-arid) and Santo Tomas</p><p>(seasonally dry). The Ci values were calculated from leaf gas fluxes via standard Gaastra equations: the</p><p>higher photosynthetic rates, the lower Ci values. Regression equation: yield = 1.52 - 0.004 Ci; r2 = 0.82</p><p>(P < 0.001). From de Tafur et al. (1997b). Permission conveyed through Copyright Clearance Center,</p><p>Inc.</p><p>Mabrouk A. El-Sharkawy</p><p>100</p><p>In late 1980 and early 1990, breeding efforts at CIAT were further integrated with the</p><p>Brazilian national institutions involved in cassava research, mainly the federal research</p><p>organizations of EMBRAPA and CNPMF, with headquarters at Cruz das Almas, Bahia State</p><p>(Fukuda et al., 1992-1993). Also, collaboration with IITA, Nigeria, took place at the same</p><p>time. As the crop physiologist at CIAT, I participated, along with CIAT breeders and the</p><p>Brazilian national cassava team, in the initiation of a research project for cassava breeding in</p><p>northeastern Brazil that was supported</p><p>by the International Fund for Agricultural</p><p>Development, Rome (El-Sharkawy, 1993). Based on the available meteorological data, four</p><p>relevant sites were pre-selected for screening cassava germplasm in northeastern Brazil,</p><p>namely: (i) Itaberaba (270 m a.s.l., 12o31΄S), Bahia. At this site, mean annual rainfall is about</p><p>718 mm, with a continuous rain throughout the year, but with two wet cycles. From January</p><p>to April total rainfall is about 332 mm. There is a shorter wet cycle from November-</p><p>December with a total rainfall of 200 mm. The rest of the year is considered dry as the</p><p>monthly rainfall oscillated between 20 to 40 mm, which is far below the potential</p><p>evaporation. (ii) Quixadá (179 m a.s.l., 4o57΄S), Ceará State. At this site, mean annual rainfall</p><p>is about 677 mm, with only a four-month wet cycle (from February to May) with a total</p><p>rainfall of 542 mm. The rest of the year is extremely dry, as monthly rainfall oscillated</p><p>between zero to 45 mm. (iii) Petrolina (376 m a.s.l., 9o22΄S), Pernambuco State. At this site,</p><p>mean annual rainfall is about 400 mm, with monthly distribution (mm) as follows: 50 in</p><p>January, 78 in February, 92 in March, 43 in April, 7 in May, 4 in June, 2 each from July to</p><p>September, 9 in October, 45 in November, 64 in December. This site is the driest among the</p><p>pre-selected sites, as illustrated by the pattern of rainfall distribution. (iv) Araripina (816 m</p><p>a.s.l., 7o32΄S), Pernambuco. This site is the wettest among the pre-selected sites with mean</p><p>annual rainfall of about 820 mm. The rainfall distribution pattern is very similar to that in</p><p>Petrolina, but with the three wetter months having a total rainfall of 422 mm (January 114,</p><p>February 134, March 174). The rest of the year was considered dry, as indicated by the</p><p>monthly rainfall distribution that oscillated between zero and 63 mm. The soils in these sites</p><p>are sandy with low water holding capacity in addition to being very low in fertility.</p><p>Cassava germplasm (500 clones) originating from northeast Brazil and the north coast of</p><p>Colombia was initially screened at these four sites for yield, HI, root dry matter content,</p><p>cyanogenic glucosides level (expressed in total HCN, concentration in storage root</p><p>parenchyma) and resistance to mites. In general, in the 1991-1992 growing season, cassava at</p><p>all sites suffered from a more severe drought than normal, with total annual rainfall less than</p><p>200 mm in Petrolina, less than 500 mm in Araripina, less than 360 mm in Quixadá. Only at</p><p>Itaberaba was rainfall about 853 mm, more than normal (Fukuda et al., 1992-1993). Despite</p><p>these harsh environments, a large number of accessions persisted and produced, while some</p><p>failed. Better drought-adapted clones established full canopy after four months and retained</p><p>leaf area up to eight months after planting (Fukuda et al., 1992-1993; El-Sharkawy, 1993). In</p><p>Table 7 the results of the preliminary screening trials as overall averages of the four sites are</p><p>summarized. Several accessions of Brazilian origin were selected with good yield potential</p><p>that ranged from 13 to 18 t ha-1 fresh roots with mean 25% dry matter. Harvest index ranged</p><p>from 0.45 to 0.55. There was tolerance to prolonged drought, as indicated by better leaf</p><p>retention and duration during most of the cropping cycle. Low HCN content was in root</p><p>parenchyma, and it ranged from 53 to 100 mg kg-1 fresh root, which are acceptable levels for</p><p>fresh root consumption. Mite resistance scores ranged from 3.3 to 2.7, based on a visually</p><p>assessed scale from 5 (highly susceptible) to 1 (highly resistant).</p><p>Cassava</p><p>101</p><p>Table 7. Clones (harvested at 12 months) with good level of adaptation to four screening</p><p>sites in semiarid northeastern Brazil. Values are averages of all sites. From</p><p>CIAT/CNPMF breeding database (1992)</p><p>Brazil accesion</p><p>code</p><p>Fresh root</p><p>yield (t ha-1)</p><p>HI</p><p>*</p><p>Root dry matter</p><p>content (%)</p><p>HCN content</p><p>(mg kg-1 FM) †</p><p>Mite</p><p>resistance</p><p>score ‡</p><p>‘BGM 538’ 18 0.50 30.1 78 2.9</p><p>‘BGM 146’ 17 0.51 28.0 85 3.0</p><p>‘BGM 178’ 16 0.44 29.1 95 3.0</p><p>‘BGM 549’ 16 0.42 28.6 72 3.1</p><p>‘BGM 537’ 15 0.48 30.4 72 2.7</p><p>‘BGM 254’ 15 0.50 28.0 90 2.9</p><p>‘BGM 544’ 14 0.55 29.1 95 3.1</p><p>‘BGM 153’ 14 0.45 28.0 100 3.1</p><p>‘BGM 598’ 13 0.47 29.0 53 2.7</p><p>‘BGM 491’ 13 0.46 27.7 60 3.3</p><p>Overall mean</p><p>of 500 clones 9 0.40 25.1 75 3.3</p><p>*HI, harvest index means the fresh root yield divided by fresh total harvested biomass excluding fallen</p><p>leaves; †, total hydrocyanic acid content in parenchyma of peeled roots. The clones with HCN</p><p>content less than 100 mg kg-1 FM are considered safe for human consumption after fresh cooking.</p><p>‡, mite resistance score: 1 (highly resistance) to 5 (highly susceptible). Higher levels of HCN are</p><p>hazardous for human health if consumed without proper processing to eliminate most of the HCN.</p><p>Table 8. Clones (harvested at 1.0 and 1.5 yr) with good level of adaptation at the</p><p>semiarid screening site in Quixadá, Ceará, northeastern Brazil, 1996. From</p><p>CIAT/CNPMF breeding database (1996)</p><p>Brazil accession Fresh Dry Dry matter content</p><p>coode root yield root yield in roots</p><p>(t ha-1) (%)</p><p>1.0 yr 1.5 yr 1.0 yr 1.5 yr 1.0 yr 1.5 yr</p><p>‘BGM 649’ 14.9 32.0 4.7 11.5 31.8 35.7</p><p>‘BGM 651’ 10.7 30.2 3.2 10.0 29.9 33.2</p><p>‘BGM 814’ 10.2 36.1 2.5 13.7 24.1 37.8</p><p>‘BGM 834’ 23.8 39.8 5.7 12.7 24.2 31.8</p><p>‘BGM 867’ 11.8 32.2 2.8 11.5 23.4 36.0</p><p>‘BGM 876’ 14.6 38.0 3.6 13.7 24.5 36.1</p><p>‘BGM 924’ 13.5 37.0 2.3 12.5 17.3 33.7</p><p>Mean of selections 14.2 35.0 3.5 12.2 25.0 34.9</p><p>Trial mean 12.7 26.6 3.2 9.2 25.2 34.5</p><p>Check cultivars mean 7.1 27.8 1.7 9.8 23.8 35.3</p><p>These preliminary trials laid the foundations for a further expanding of the breeding</p><p>project based on a scheme for producing hybrids via crossing among various selected clones</p><p>with a range of desirable traits under semiarid conditions (Fukuda et al., 1992-1993). Further</p><p>Mabrouk A. El-Sharkawy</p><p>102</p><p>on-farm trials involving farmers in the process of evaluation of breeding materials have</p><p>resulted in a few selected genotypes with higher yields, compared to local checks (Table 8).</p><p>When left for a second wet cycle in semiarid low-rainfall locations, fresh yields more than</p><p>doubled (from an average yield of 14 t ha-1 at 12 months to 35 t ha-1 at 18 months). The dry</p><p>matter contents in fresh roots increased from 25% at 12 months to 35% at 18 months, which</p><p>led to more than three-fold increases in dry root yields (from an average of 3.5 t ha-1 at 12</p><p>months to 12.2 t ha-1 at 18 months). Farmers adopted some of these improved genotypes and</p><p>started multiplying planting material even before being officially released. In these semiarid</p><p>environments drought-tolerant grain crops such as sorghum and millets (Blum and Sullivan,</p><p>1986) will fail to produce as much, indicating the comparative advantages of cassava. This</p><p>research is a remarkable example of interdisciplinary/interinstitutional collaborative efforts</p><p>that serve the needs of some of the poorest farmers in the tropics.</p><p>FUTURE WORK</p><p>The aim of the physiological research conducted at CIAT was to apply it at the field level</p><p>as well as to translate the findings into improved technology for the benefits of the farmers, a</p><p>challenge that most plant physiologists have to face and endure in many research and</p><p>development institutions in developed countries. This challenge becomes almost</p><p>insurmountable in developing countries where basic research has low priority in national</p><p>agricultural research systems. The time span of the CIAT research was relatively short under</p><p>restrictive financial support. Yet, application of the gained physiological knowledge, as</p><p>summarized above, into breeding new improved cultivars took place simultaneously during</p><p>the course of the research involved (see Cock and El-Sharkawy, 1988; El-Sharkawy et al.,</p><p>1990, 2008; Hershey and Jennings, 1992; CIAT, 1993; El-Sharkawy,</p><p>1993, 2004; Iglesias et</p><p>al., 1995; Iglesias and Brekelbaum, 1996; de Tafur et al., 1997b; Jennings and Iglesias, 2002;</p><p>Lenis et al., 2006). For example, one short-stemmed cultivar, tolerant to drought with a stable</p><p>yield and very high dry matter content in storage roots, was selected from trials conducted in</p><p>Colombia and further tested in semi-arid areas of Ecuador (see CIAT, 1993; El-Sharkawy et</p><p>al., 2008). It was successfully accepted by farmers, who had participated in its evaluation on</p><p>several field-trials, and now is widely cultivated under the local name ‘Portoviejo 650’. The</p><p>same achievements occurred in Colombia and Brazil as pointed above.</p><p>Nevertheless, two areas of future research and development need to be addressed on the</p><p>potential use of cassava as a mainstay crop tolerant to extreme water deficits and to marginal</p><p>lands in the tropics and subtropics where severe drought prevails and shortages of food and</p><p>feed are chronic, particularly in sub-Saharan Africa: (i) Through the use of modern molecular</p><p>biology tools, more basic research on cassava biochemical photosynthetic characterization</p><p>should be done to search for genetic diversity within cultivated cassava and wild Manihot</p><p>species in order to identify genetic sources with high photosynthetic capacities and enhanced</p><p>activities of key photosynthetic enzymes, focusing on PEPC and C3-C4 traits (El-Sharkawy</p><p>and de Tafur, 2007; El-Sharkawy et al., 2008). Also, the molecular basis for tolerance to</p><p>water stress and identification of possible controlling genes should be investigated using</p><p>contrasting germplasm as well as wild species (e.g. Lokko et al., 2007). The use of molecular</p><p>markers and marker-assisted selection should further facilitate and enhance the conventional</p><p>Cassava</p><p>103</p><p>breeding process for drought-tolerance in cassava (Setter and Fregene, 2007). This line of</p><p>research should be internationally supported within an interdisciplinary/interinstitutional</p><p>collaborative network, including research institutes in developed countries. (ii) National</p><p>programs, perhaps supported with the Geographical Information Systems, should make the</p><p>necessary mapping of additional new lands and suitable climatic conditions for potential</p><p>expansion in cassava production where other staple food crops will probably fail to produce.</p><p>Application of the Geographical Information Systems has shown its utility in identifying</p><p>potential lands suitable for cassava production in semi-arid sub-Saharan Africa (e.g. El-</p><p>Sharkawy, 1993). This effort should be continued and backed up by developing the necessary</p><p>adapted cultivars endowed with early storage root filling characteristics (i.e. early bulking</p><p>cultivars suitable for semi-arid areas) and better leaf retention (Lenis et al., 2006) and</p><p>duration coupled with resistance to pests and diseases. Agronomic/physiological research in</p><p>the area of plant-soil-water relations and plant nutrition on the newly bred cultivars would</p><p>provide the technical knowledge needed for cropping systems and natural resources</p><p>managements. Crop modeling, based on sound field research, should play a role in integrating</p><p>crop ecophysiology, agroclimatology, and genomics information in this case (Pan et al., 2000;</p><p>El-Sharkawy, 2005; Long et al., 2006; Begonia and Begonia, 2007; Steiner and Hatfield,</p><p>2008; Yin and Struik, 2008).</p><p>CONCLUSION</p><p>The research on cassava summarized in this chapter illustrates the effectiveness and</p><p>utility of ecophysiological research in improving the genetic base and in developing</p><p>genotypes more adaptable to drought in the marginal environments in the tropics. Linking and</p><p>integrating physiological research with breeding efforts within a commodity-oriented</p><p>multidisciplinary research team at CIAT, and in collaboration with national programs, were</p><p>pivotal in delivering the needed information and improved technology. Plant traits related to</p><p>productivity and to tolerance to water stress, such as high leaf photosynthetic capacity and</p><p>longer leaf life and duration, extensive fine rooting systems and stomatal control of water</p><p>losses, were identified and selected for parental materials used in breeding for improved and</p><p>more adaptable genotypes. Furthermore, the research has revealed important information on</p><p>the physiological mechanisms underlying cassava productivity and tolerance to prolonged</p><p>drought that should help to develop better crop management in both favorable and stressful</p><p>environments. More research is needed to elucidate further the biochemical and molecular</p><p>characteristics of cassava photosynthesis in relation to productivity, particularly under stress.</p><p>This would require essential changes in the current counterproductive policy of the</p><p>international research system, which is based on short-term research projects that do not</p><p>ensure needed solutions to farmers problems. This policy should be reversed and replaced by</p><p>the previously adopted and more effective long-term core funding of interdisciplinary and</p><p>integrated research approach (El-Sharkawy, 2006a, 2006b). National programs should be</p><p>responsible for conducting the applied and adaptive research aspects that are required for</p><p>fulfillment of their national needs.</p><p>Across institutions and countries, collaborative research, as that illustrated by the project</p><p>conducted by CIAT and EMBRAPA/CNPMF, Brazil, on breeding improved cassava cultivars</p><p>Mabrouk A. El-Sharkawy</p><p>104</p><p>for the seasonally dry and semiarid environments, should not only be encouraged but also</p><p>emulated in other crops. In view of the adverse effects on agricultural productivity in tropical</p><p>countries that might result from observed global climate changes, more research on drought</p><p>tolerance is warranted. Cassava, with its inherent capacity to tolerate and produce reasonably</p><p>well under prolonged drought, should be expected to provide more essential food and feed</p><p>than any other crop in marginal environments.</p><p>ACKNOWLEDGMENTS</p><p>I am grateful for the sincere collaboration I received during the course of this research</p><p>from the many workers, colleagues, associates, visiting scientists, students, secretaries at</p><p>CIAT, and the Colombian farmers who generously offered logistic support and hospitality at</p><p>their private farms and homes. The financial grants from The International Fund for</p><p>Agricultural Development, Rome, helped in initiating the collaborative breeding project</p><p>between CIAT and the federal research organizations in Brazil (EMBRAPA/CNPMF) in</p><p>seasonally dry and semiarid areas of northeastern Brazil. Without this support, the</p><p>achievements highlighted here would have never been realized. I am also thankful to my</p><p>daughter, Farah El-Sharkawy Navarro, for her support in organizing the data in tables and</p><p>figures and in searching the internet for needed information and references. The invaluable</p><p>inputs provided by Dr. Mary B. Kirkham, Kansas State University, Manhattan, Kansas, were</p><p>also appreciated.</p><p>REFERENCES</p><p>Aguilar LP. Ultraestructura foliar y fotosíntesis de yuca en diferentes cultivares (Manihot</p><p>esculenta Crantz). BSc thesis, Universidad de Cauca, Popayan, Colombia; 1995.</p><p>Allem AC. The origin and taxonomy of cassava. 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Protein contents, amino acid composition and nitrogen-to-protein</p><p>conversion factors for cassava roots. J. Sci. Food Agric. 1996;70:51-4.</p><p>In: Ecophysiology of Tropical Tree Crops ISBN 978-1-60876-392-4</p><p>Editor: Fabio DaMatta © 2010 Nova Science Publishers, Inc.</p><p>Chapter 5</p><p>CITRUS: AN OVERVIEW OF FRUITING PHYSIOLOGY</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores,</p><p>Miguel A. Naranjo, Gabino Ríos, Esther Carrera,</p><p>Omar Ruiz-Rivero, Ignacio Lliso, Raphael Morillon,</p><p>Francisco R. Tadeo and Manuel Talon</p><p>ABSTRACT</p><p>Citrus (Citrus spp.) is the main fruit tree crop in the world and therefore has a</p><p>tremendous economical, social and cultural impact in our society. In recent years, our</p><p>knowledge on plant reproductive biology has increased considerably mostly because of</p><p>the work developed in model plants. However, the information generated in these species</p><p>cannot always be applied to citrus, predominantly because citrus is a perennial tree crop</p><p>that exhibits a very peculiar and unusual reproductive biology. Regulation of fruit growth</p><p>and development in citrus is an intricate phenomenon depending upon many internal and</p><p>external factors that may operate both sequentially and simultaneously. The elements and</p><p>mechanisms whereby endogenous and environmental stimuli affect fruit growth are being</p><p>interpreted and this knowledge may help to provide tools that allow optimizing</p><p>production and fruit with enhanced nutritional value, the ultimate goal of the Citrus</p><p>Industry. In this chapter we review the progress that has taken place in the physiology of</p><p>citrus fruiting during recent years and present the current status of major research topics</p><p>in this area.</p><p>INTRODUCTION</p><p>Fruit have been a matter of extensive research in recent years because of their importance</p><p>to agriculture and the human diet. However, research on fleshy fruit has focused primarily on</p><p>climacteric fruits such as tomato while other fruit models are not so well known. In this</p><p>chapter, we will review our understanding of citrus fruit development and will present it as a</p><p>plausible model for tree and woody perennials. We will focus on the physiology of citrus</p><p>fruiting, an area that complements the information presented in two recently published</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>112</p><p>reviews dealing with the generation of genomic tools and resources (Talon and Gmitter,</p><p>2008) and the progress in molecular biology and genetics of development (Tadeo et al., 2008)</p><p>in the genus Citrus. The focus chosen for this chapter is on major physiological factors</p><p>regulating fruit growth including flowering, hormones, carbohydrates, and abiotic constrains.</p><p>Also revised are major biochemical aspects of the ripening processes that may be important</p><p>for fruit quality. A central part of the chapter concentrates on the hormonal and metabolic</p><p>control of fruit set and development and documents progress in the understanding of</p><p>abscission processes.</p><p>ECONOMICAL AND SOCIAL RELEVANCE</p><p>Citrus is the most economically important fruit crop in the world, is grown in developed</p><p>and developing countries and certainly constitutes one of the main sources of vitamin C.</p><p>There is also an increasing demand of “high quality fresh citrus” driven by World Health</p><p>Organization recommendations. Citrus contain the largest number of carotenoids found in any</p><p>fruit and an extensive array of secondary compounds with pivotal nutritional properties such</p><p>as vitamin E, pro-vitamin A, flavonoids, limonoids, polysaccharides, lignin, fiber, phenolic</p><p>compounds, essential oils etc. These substances greatly contribute to the supply of anticancer</p><p>agents and other nutraceutical compounds with anti-oxidant, anti-inflammatory, anti-</p><p>cholesterol and anti-allergic activities, all of them essential to prevent cardiovascular and</p><p>degenerative diseases, thrombosis, cancer, atherosclerosis and obesity. In spite of these</p><p>beneficial traits there is still a major need to improve fruit quality to meet current consumer’s</p><p>demands.</p><p>Reproductive Biology</p><p>From a scientific standpoint, citrus has proved to be valuable material for studying many</p><p>biological questions because citrus combine an unusual mixture of reproductive characteristics</p><p>including, for example, non-climacteric development. In contrast to climacteric fruits (reviewed</p><p>in Giovannoni, 2004), the mechanism of ripening in non-climacteric fruits is basically</p><p>unknown. Citrus also exhibit a long juvenility phase and nearly all important citrus species</p><p>including sweet oranges, mandarins, lemons and grapefruits show some degree of apomixis.</p><p>Furthermore, many of them are parthenocarpic, sterile or self-incompatible and/or develop</p><p>defective pollen (Baldwin, 1993; Davies and Albrigo, 1994). In seeded citrus cultivars, fruit</p><p>development is linked to the presence of seeds and, therefore, it depends upon pollination and</p><p>fertilization. Self-pollination usually</p><p>takes place in the unopened or opening flower, often</p><p>allowing pollination before anthesis. Cross-pollination occurs between plants of different</p><p>genetic background by insect transport of pollen. However, many current citrus cultivars are</p><p>mostly seedless varieties showing high parthenocarpy, in many instances due to gametic</p><p>sterility. Generative sterility can be relative or absolute. Relative gametic sterility may be due</p><p>to self-incompatibility as in ‘Clementine’ and to cross-incompatibility. On the other hand,</p><p>absolute gametic sterility is associated with pollen and/or embryo-sac sterility. Some cultivars</p><p>Citrus: An Overview of Fruiting Physiology</p><p>113</p><p>such as ‘Washington Navel’ oranges and ‘Satsuma’ mandarins have both, although even in</p><p>these two varieties a few embryo sacs may often reach maturation.</p><p>Citrus fruits are also classified as hesperidiums, berries of very special organization</p><p>characterized by a juicy pulp made of vesicles within segments. Thus, the combination of</p><p>these characteristics suggests that the study of citrus fruit growth may reveal original</p><p>regulation mechanisms based on specific molecular differences and/or even novel genes</p><p>(Forment et al., 2005; Cercós et al., 2006; Terol et al., 2007).</p><p>Citrus fruits are particularly convenient models to study regulation, for example, of</p><p>secondary metabolism or sugar and citric acid build-ups. Although many efforts have been</p><p>certainly dedicated to comprehensive physiological and biochemical descriptive studies (see</p><p>Baldwin, 1993) there is still an enormous unexplored potential in the study of the regulation of</p><p>the metabolites associated with citrus fruit growth.</p><p>CITRUS FRUIT SET AND GROWTH</p><p>Fruit Growth and Abscission</p><p>In general, fruit formation in citrus pursues a genetic developmental program expressed</p><p>over a relatively long period. In most species under subtropical conditions flowering takes</p><p>place in spring and the subsequent formation of fruit extends until mid-winter. However, full</p><p>ripening in early varieties may be reached as soon as September while in late species it can be</p><p>prolonged until the onset of next summer. Growth and development of citrus fruit follows a</p><p>typical sigmoid growth curve, divided into three clear-cut stages (Bain, 1958). The initial</p><p>phase, or phase I, is an approximately two-month interval of cell division and slow growth</p><p>including the period between anthesis and June drop. Thereafter, in the rapid growth period</p><p>(phase II) fruit experiences a huge increase in size by cell enlargement and water</p><p>accumulation during four to six months. Therefore, developing fruitlets are utilization sinks</p><p>during the cell division period and act rather as storage sinks during phase II (Mehouachi et</p><p>al., 1995). Finally, in phase III or ripening period growth is mostly arrested and fruits undergo</p><p>a non-climacteric process.</p><p>Citrus bloom profusely and therefore also show high abscission of buds, flowers, fruitlets</p><p>and fruits. It is interesting to note that although abscission of reproductive organs is overall</p><p>continuous during phase I, two waves of elevated abscission take place at the onset of phase I</p><p>and during the transition to phase II. Thus, bud, flower and ovary abscission occurs mostly at</p><p>the beginning of the cell division phase, whereas fall of fruitlets and developing fruits is</p><p>higher during the June drop. Generally, a small percentage of fruits overcome the June drop</p><p>and in general less than 1% reaches ripening. The period in which fruit is liable to fall is</p><p>referred to as fruit set and in this episode that can be extended along the whole phase I,</p><p>several endogenous and exogenous factors configure the decision of either setting or aborting</p><p>growth. The end of the period of fruit set usually coincides with the metabolic transition from</p><p>cell division to cell enlargement. During phase II and phase III fruit abscission is considerably</p><p>reduced although in some species and under adverse environmental conditions ripe fruits may</p><p>show pre-harvest fall. Furthermore, in many varieties overripe fruit is quite insensitive to</p><p>abscission. In citrus trees, flower and ovary abscission generally occurs through abscission</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>114</p><p>zone A (AZ A, between the twig and the peduncle) that becomes progressively inoperative</p><p>during phase I while abscission in zone C (AZ C, in the calyx between the ovary wall and the</p><p>nectary) is activated during June drop and at ripening.</p><p>Regulation of Fruit Set and Growth</p><p>In seeded citrus, activation of the genetic programs regulating early growth and set</p><p>depends mostly upon external stimuli of environmental nature, such as pollination, and hence</p><p>of bloom quality. Aside from flowering intensity and the type of inflorescence, other major</p><p>regulating factors can also be visualized since in seedless cultivars the initiation of these</p><p>programs appears to be linked to the development. Although this proposal implies different</p><p>kinds of control, many of them are probably operating through the synthesis and action of the</p><p>same hormonal messengers. After activation, fruit growth is apparently supported by the</p><p>availability of nutrients mostly mineral elements, carbohydrates and water. However,</p><p>carbohydrate supply for the flower or fruit load is often insufficient and also favorable</p><p>environmental conditions may eventually become adverse. Under these circumstances, new</p><p>hormonal signals are generated to trigger temporal protection mechanisms, for example,</p><p>stomata closure and growth arrest or even more drastic responses such as organ abscission.</p><p>Therefore, the control of fruit growth and abscission in citrus is a complex phenomenon under</p><p>at least three levels of regulation: genetic, metabolic and environmental. The distinct levels of</p><p>regulation may act sequentially, simultaneously or can be superimposed on each other,</p><p>although all three appear to operate partially through hormonal signals. Below, main</p><p>physiological factors affecting fruit set and development are revised.</p><p>Citrus Flowering</p><p>Citrus species show a relatively long juvenility period (2 to 5 yr) before the trees reach</p><p>the mature stage to produce flowers. The inflorescence developed in citrus may be either</p><p>leafless or leafy and these may carry a single flower or several of them (Goldschmidt and</p><p>Huberman, 1974). The ratio of each kind of inflorescence in the tree varies with flowering</p><p>intensity and cultivar. For example, high flowering intensities are generally related to high</p><p>rates of leafless floral sprouts although some cultivars, such as ‘Satsuma’ (C. unshiu Marc.)</p><p>that tends to produce only vegetative shoots and single flower inflorescences, may show some</p><p>particularities.</p><p>Citrus species usually produce a large number of flowers over the year. The floral load</p><p>depends on the cultivar, tree age and environmental conditions (Monselise, 1986). It has been</p><p>reported, for example, that sweet oranges (C. sinensis) may develop 250,000 flowers per tree</p><p>in a bloom season although only a small amount of these flowers (usually less than 1%)</p><p>becomes mature fruit (Erickson and Brannaman, 1960; Goldschmidt and Monselise, 1977).</p><p>Thus, flowering represents a great input for citrus trees and to some extent even a waste of</p><p>resources. For some authors, however, this reproductive pattern may be linked to a survival</p><p>strategy (Bustan and Goldschmidt, 1998).</p><p>Citrus: An Overview of Fruiting Physiology</p><p>115</p><p>Flowering Induction</p><p>In subtropical regions, citrus major bloom occurs during the spring flush along with the</p><p>vegetative sprouting. Under these environmental conditions, flowering takes place after a</p><p>period of bud quiescence and the exposure to the low temperatures and short days of winter</p><p>(Figure 1). Generally, summer and fall flushes are less intense and produce almost</p><p>exclusively vegetative shoots. The importance of temperature as a major factor of flower</p><p>induction is well established</p><p>and has been recognized for a long time (Moss, 1969; Altman</p><p>and Goren, 1974; Guardiola et al., 1982; Valiente and Albrigo, 2004; Nebauer et al., 2006).</p><p>Several authors have proposed that low temperatures may have a dual effect releasing bud</p><p>dormancy and inducing flowering (Southwick and Davenport, 1986; García-Luis et al. 1989,</p><p>1992; Tisserat et al., 1990). Moreover, temperatures under 20ºC have been demonstrated to</p><p>contribute to flower bud induction in a time dependent manner (Moss, 1969; Southwick and</p><p>Davenport, 1986; García-Luis et al., 1992).</p><p>In tropical climates, however, bud sprouting and flowering come about without</p><p>interruption throughout the year although the main bloom still occurs during the spring</p><p>(Monselise, 1985; Spiegel-Roy and Goldschmidt, 1996). In contrast to the sub-tropical</p><p>stimuli, in tropical conditions citrus apparently flower in response to drought periods. In</p><p>addition to low temperature, water deficit has also been recognized for a long time as another</p><p>strong inductor of flowering in citrus (Cassin et al., 1969). Moreover, water deficit has been</p><p>proved to increase the ratio of floral shoots and the total number of flowers (Southwick and</p><p>Davenport, 1986).</p><p>It should be noted that several citrus species and varieties also show a wide range of</p><p>behaviors regarding both flowering time and response to the inductive conditions. For</p><p>example, lemon trees tend to show sparse flowering over the year even in subtropical</p><p>conditions (Nir et al., 1972) and also exhibit higher floral responses to waters stress than to</p><p>cold inductive temperatures (Chaikiattiyos et al., 1994). This effect has been commercially</p><p>used to induce off-season flowering (Davies and Albrigo, 1994).</p><p>There are many instances suggesting that the flowering response to inductive conditions</p><p>is also influenced by endogenous factors. For example, citrus buds on previous summer</p><p>shoots and buds at apical positions produce more flowers than older or lateral buds (Valiente</p><p>and Albrigo, 2004). It is also well known that the fruit load has a strong negative effect on</p><p>spring sprouting of both vegetative and generative buds and therefore constitutes a major</p><p>inhibitor of flowering. Conversely, the absence of fruit or a scarce fruiting induces huge</p><p>flowering intensities in the next season. Thus, crop load is likely the main cause of the</p><p>“alternate bearing” behavior of many citrus species and varieties including many seeded</p><p>mandarins that alternate reduced flowering and fruiting (“off year”) with increased flower</p><p>induction and fruit production (“on year”). From an agronomical point of view, undesirable</p><p>flowering behaviors such as alternate bearing may be partially alleviated by different</p><p>treatments inhibiting or promoting flower production. The flowering response to fruit load</p><p>has been attributed to carbon shortage that provokes the presence of fruit and/or to the release</p><p>of signaling compounds, mainly gibberellins from the ripe fruits (Monselise, 1985; Garcia-</p><p>Luis et al., 1986; Erner, 1988; Koshita et al., 1999).</p><p>The role of sugars on flowering induction is mostly supported by circumstantial evidence.</p><p>For example, it is known that “girdling”, the removal of a bark ring, increases flower</p><p>induction and it has been suggested that this stimulating effect is due to the transitory block of</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>116</p><p>phloem flux that apparently increases sugar availability in the aerial parts of the tree</p><p>(Wallerstein et al., 1978; Yamanishi, 1995).</p><p>Figure 1. Regulation of citrus flowering. In subtropical regions, citrus bloom generally occurs during</p><p>the spring flush along with vegetative sprouting. In these areas, flowering takes place after a period of</p><p>bud quiescence and the exposure to the low temperatures and short days of winter. In tropical regions</p><p>and in areas with drought seasons citrus also flower in response to re-hydration after a period of water</p><p>deficit. Huge fruit load, leaf removal and exogenous gibberellic acid reduce flowering, normally</p><p>decreasing the rate of leafless shoots. The probability of fruit set, represented as a downward arrow, is</p><p>inversely related to the number of flowers within the shoot. From Iglesias et al. (2007) with permission</p><p>of Brazilian Society of Plant Physiology.</p><p>Gibberellin (GA) treatment is a common agricultural practice that is currently used to</p><p>inhibit flowering in citrus trees. Applications of gibberellic acid during citrus bud</p><p>development have been widely shown to inhibit flower production (Guardiola et al., 1982),</p><p>leading to a greater ratio of terminal flowers in leafy shoots and consequently a higher fruit</p><p>development. This observation is in contrast to the reported flowering promoting effect of GA</p><p>on annual plants such as Arabidopsis thaliana. Despite the absence of a mechanism to cope</p><p>with this observation, the flower repressing effect of gibberellins is corroborated by</p><p>treatments with the inhibitor of GA biosynthesis paclobutrazol, which consistently induces</p><p>flowering when applied to the field. Furthermore, the treatments with GA synthesis</p><p>antagonists are not effective when GA is already present at high levels. Bud treatments with</p><p>GAs also reduce summer bud sprouting (Lliso et al., 2004). Other growth regulators and</p><p>phytohormones have also been assayed with variable results. Benzyladenine, for instance, has</p><p>been suggested to have a specific effect on flower differentiation (Iwahori et al., 1990) and to</p><p>promote general bud sprouting in vitro (Altman and Goren, 1978) and in whole trees (Nauer</p><p>and Boswell, 1981; Lliso et al., 2004).</p><p>Citrus: An Overview of Fruiting Physiology</p><p>117</p><p>Plant nutrition status has also been associated with citrus flowering. Higher contents of N</p><p>(ammonia), in particular, in the buds and leaves altered by winter application of urea</p><p>increased the number of flowers per tree (Lovatt et al., 1988; Albrigo, 1999). Similarly, N</p><p>fertilization over 3 yr has been shown to improve canopy width and flower yield (Menino et</p><p>al., 2003).</p><p>Recently, molecular mechanisms regulating flowering in citrus were investigated in</p><p>relation to DNA methylation in buds but no clear, conclusive results were reported (Nebauer</p><p>et al., 2006).</p><p>Leafy Versus Leafless Inflorescences</p><p>Although citrus species may show some differences in the initiation of flower formation</p><p>(Abbot, 1935), floral differentiation has been reported to occur close to the end of the cold</p><p>season, just at bud sprouting (Guardiola et al., 1982; Lord and Eckard, 1985). Actually, the</p><p>first morphological differences between reproductive or vegetative buds are only observable</p><p>at this moment (Davenport, 1990). Citrus fruit set is highly dependent upon the type of</p><p>inflorescence. In general, leafless inflorescences emerge first and contain a bouquet of</p><p>flowers with low probability to set fruit. On the other hand, flowers in leafy inflorescences</p><p>that can be terminal or distributed among leaves along the shoot are commonly associated</p><p>with higher fruit set (Jahn, 1973). Usually, late-opening flowers remain attached to the tree</p><p>longer than early-opening flowers and flowering shoots with a high leaf-to-flower ratio have</p><p>the highest fruit set (Lovatt et al., 1984). The positive influence of leaves on fruit set appears</p><p>to be associated with increased net CO2 assimilation and supply of photoassimilates from</p><p>developing leaves (Syvertsen and Lloyd, 1994). These might also influence ovary growth and</p><p>fruit set through the provision of GAs since leafy inflorescences contain higher hormonal</p><p>levels than leafless ones (Ben-Cheikh and Talon, unpublished results).</p><p>Pollination and parthenocarpy</p><p>In general, fruit set also depends on successful pollination and fertilization since the</p><p>presence of fertilized ovules normally triggers fruit development. In seeded citrus, the</p><p>decision to initiate fruit development certainly requires pollination and fertilization. If the</p><p>flower is not pollinated,</p><p>the development of the gynoecium arrests, the whole flower senesces</p><p>and eventually abscises. In the seeded sweet orange cultivars of ‘Pineapple’ for example, lack</p><p>of fertilization will inevitably lead to abscission of the ovary since all emasculated and non-</p><p>pollinated flowers arrested growth and fell shortly after anthesis (Ben-Cheikh et al., 1997).</p><p>Growth arrest of unpollinated ovaries is mostly due to a failure in the re-activation of cell</p><p>division as is seen in the pollinated fruitlet (Ben-Cheikh et al., 1997). Thus, fruit set in this</p><p>cultivar is strictly dependent on pollination and fertilization. The duration of the bloom period</p><p>is linked to temperature regimen (Spiegel-Roy and Goldchmidt, 1996). High temperatures</p><p>accelerate anthesis and shorten the bloom period while low temperatures lead to an extended</p><p>flowering period (Lovatt et al., 1984; Bellows and Lovatt, 1989; Davenport, 1990). Thus,</p><p>temperature conditions may have important consequences for the chances of pollination and</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>118</p><p>fruit set. Temperature also affects the activity of bees, the main citrus pollinators, and the</p><p>growth rate of pollen tubes. Under standard temperature conditions, the effective pollination</p><p>period varies in citrus cultivars between 8-9 d for sweet oranges and ‘Clementine’ mandarins</p><p>to 2-3 d for ‘Satsuma’ mandarins (Mesejo et al., 2007). In addition to temperature, several</p><p>other factors such as flower number (Moss, 1973; Valiente and Albrigo, 2004), inflorescence</p><p>type, floral position (Lovatt et al., 1984) and nutritional status may also affect flower</p><p>formation and development and therefore fruit set.</p><p>However, many current commercial citrus cultivars are seedless varieties since their fruit</p><p>are often well appreciated for their ease of consumption. There are also several classes of</p><p>seedlessness in commercially available citrus fruit ranging from self-incompatible cultivars</p><p>such as ‘Clementine’ mandarin that show a lower ability to set fruit in the absence of cross-</p><p>pollination to the truly seedless Satsuma mandarins and ‘Navel’ sweet oranges, that generally</p><p>set a normal crop of parthenocarpic fruit, due to high masculine and feminine gametic sterility</p><p>(Frost and Soost, 1968). In these varieties, parthenocarpic fruit develop without formation of</p><p>seeds and therefore all pollination, fertilization or seed requirements for fruit growth</p><p>activation have clearly been substituted by endogenous signals. Self-incompatible cultivars</p><p>show a low degree of parthenocarpy and therefore can be considered to possess “facultative</p><p>parthenocarpy” meaning that seedless fruit form only when fertilization does not occur.</p><p>Hormonal Regulators of Fruit Growth and Abscission</p><p>Early reproductive processes in citrus are strongly affected by plant growth regulators</p><p>indicating that the regulatory mechanism controlling set and abscission of ovaries and fruitlets</p><p>possesses a pivotal hormonal component (Talon et al., 1990b). Overall, these studies suggest</p><p>that a complex set of hormonal interactions occur during fruit development. Thus, GAs and</p><p>cytokinins are generally considered to be positive regulators of fruit growth while auxins have</p><p>been reported to act as stimulators of growth and also as abscission agents. Abscisic acid</p><p>(ABA) and ethylene have been implicated in several ways in abscission.</p><p>Gibberellins: Gibberellins are thought to be pivotal effectors responsible for the ovary-</p><p>fruit transition (Talon et al., 1992; Ben-Cheikh et al., 1997). Gibberellins activate cell division</p><p>and cell enlargement processes in vegetative organs (Talon et al., 1991) and therefore are</p><p>generally associated with the initiation of growth (Talon and Zeevaart, 1992). The</p><p>endogenous GAs found in citrus fruits are mainly members of the 13-hydroxylation pathway</p><p>[GA53, GA97, GA44, GA17, GA19, GA20, GA29, GA1, epi-GA1, and GA8 (Goto et al., 1989;</p><p>Turnbull, 1989; Talon et al., 1990a, 1992)] leading to GA1, the bioactive GA (Zeevaart et al.,</p><p>1993). This pathway also operates in vegetative tissues of citrus (Vidal et al., 2001, 2003)</p><p>where is thought to control shoot growth and elongation (Fagoaga et al., 2007). Developing</p><p>fruits also contain at lower levels 3ß- and non-hydroxylated GAs, such as GA4, GA24, GA25,</p><p>and GA9. It is generally accepted that GAs are involved in set and development of citrus</p><p>fruits. The support for this proposal comes from several studies reporting that exogenous GA3</p><p>considerably improves parthenocarpic fruit set and growth of self-incompatible genotypes</p><p>such as ‘Clementine’ that in the absence of cross-pollination show negligible parthenocarpic</p><p>fruit set (Soost and Burnett, 1961). Later, it was found that these genotypes also contain lower</p><p>GA1 levels than the seedless varieties that show natural parthenocarpy (Talon et al., 1992). In</p><p>Citrus: An Overview of Fruiting Physiology</p><p>119</p><p>developing fruits, the GA1 levels are low just before and after anthesis and approximately</p><p>double at anthesis. This transitory rise in GA1 levels can be detected in seeded genotypes as</p><p>well as in seedless cultivars possessing high or normal ability for setting (Talon et al., 1990).</p><p>In seeded cultivars, GA increases at anthesis are therefore induced by pollination whereas in</p><p>parthenocarpic species the rise is developmentally regulated. The intensity of abscission</p><p>during the initial phases of growth is also related to the phenology of flowering. Interestingly,</p><p>the presence of leaves increases GA1 levels (Ben-Cheikh and Talon, unpublished results) and</p><p>the chances of setting (Lovatt et al., 1984). In seeded cultivars, pollination stimulates</p><p>hormonal synthesis and, therefore, increases GA1 levels in developing ovaries (Ben-Cheikh et</p><p>al., 1997). It has also been shown that in seeded varieties exogenous GA arrested fruit drop of</p><p>non-pollinated ovaries. Collectively, these observations indicate that the increase in GA1</p><p>detected in mature ovaries shortly after pollination is a signaling stimulus of the regulatory</p><p>mechanism that reactivates fruit development after anthesis.</p><p>Cytokinins: Cytokinins are also factors stimulating cell division. Increases in their levels</p><p>have also been found in developing ovaries at anthesis (Hernández and Primo-Millo, 1990),</p><p>as reported for GAs. In addition, exogenous cytokinins have been reported to enhance</p><p>parthenocarpic fruit development and stimulate sink strength in developing fruits of certain</p><p>cultivars, although these regulators are not commercially used to improve fruit set in citrus.</p><p>Auxins: These regulators have often been reported either to delay or to induce fruit</p><p>abscission, and hence may operate as growth hormones or as abscising agents. On one hand,</p><p>auxins promote cell enlargement rather than cell division. Although endogenous auxins also</p><p>increase in developing ovaries, it is well established that exogenous treatments do not</p><p>improve fruit set. Auxins are also high during the beginning of phase II, the period of cell</p><p>elongation, and it is at this moment when exogenous auxins are effective increasing fruit size</p><p>(Coggins and Hield, 1968). These observations may suggest that auxins are related to cell</p><p>enlargement, the essential factor controlling fruit size during the phase of rapid growth. The</p><p>enlargement of the auxin-treated fruits is apparently due to cell expansion rather than to cell</p><p>division. In tomato, for example, it has been postulated that auxins are part of the hormonal</p><p>signaling transduction network controlling cell expansion (Catala et al., 2000). On the other</p><p>hand, auxins may act either as delaying or accelerating agents of abscission. During the initial</p><p>phases of abscission auxins operate as inhibitors, but once the process has been initiated</p><p>auxins appear to stimulate abscission. Here, auxins could operate through the promotion of</p><p>ethylene synthesis. It has also been suggested that the causal reason of the dual effect of</p><p>auxins on leaf abscission</p><p>may conveniently be explained by the auxin-gradient concept: auxin</p><p>coming from the leaf would tend to delay abscission, whereas auxin moving down the stem</p><p>might promote abscission. In citrus, synthetic auxins increase abscission of developing</p><p>fruitlets during the cell division period. Auxin applications at the beginning of the cell</p><p>enlargement period have minor effects on fruit abscission and may result in fruit size</p><p>increase. The prevention or retardation effects of auxins on abscission can be perceived,</p><p>however, at later stages. At the end of phase II or at the onset of phase III, synthetic auxins</p><p>are commercially used to prevent or delay eventual pre-harvest fruit drop (e.g. Agustí et al.,</p><p>2002).</p><p>Abscisic acid: Although many field experiments have demonstrated that ABA does not</p><p>cause abscission when applied to the aerial part of the plant, many observations suggest that</p><p>ABA, in addition to ethylene, is implicated in the process of abscission (Goren, 1993).</p><p>Abscisic acid is high in developing ovaries at petal fall and during the June drop, at the</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>120</p><p>transition from cell division to cell enlargement. Interestingly, these two ABA increases</p><p>coincide with the abscission waves occurring at the onset of phases I and II. This hormone is</p><p>also high over periods of lower humidity, dehydration and salt or drought conditions (Gomez-</p><p>Cadenas et al., 2003a; Mehouachi et al., 2005; Agustí et al., 2007).</p><p>Ethylene: At the beginning of the past century, ethylene was identified as the component</p><p>responsible for several adverse effects on plant growth including the induction of abscission.</p><p>In the 1960’s it was generally accepted that plants could produce significant amounts of</p><p>ethylene (Brown, 1997). In citrus, the involvement of ethylene in abscission has also been</p><p>recognized for a long time (Goren, 1993). It has also been shown that ethylene is the pivotal</p><p>hormonal factor promoting the processes of leaf abscission (Tudela and Primo-Millo, 1992).</p><p>Hormonal balances: One of the current hypotheses on the hormonal regulation of</p><p>abscission suggests that the balance between specific plant growth regulators at the abscission</p><p>zone controls cell separation processes and eventually fruit drop (Addicott, 1982; Goren,</p><p>1993; Brown, 1997). In citrus organs, the effect of the auxin/ethylene balance, for example,</p><p>has been largely associated with the abscission of fruit, leaves and flowers. Thus, it has been</p><p>suggested that auxin levels must fall below a certain threshold in the citrus abscission zone</p><p>before ethylene can stimulate abscission (Goren, 1993). In another example, the crucial factor</p><p>controlling abscission appears to be the balance between indole-acetic (IAA) acid and ABA</p><p>in the fruit abscission zone (Cooper and Henry, 1972). Thus, during the fruit-harvesting</p><p>season of sweet oranges, the abscission response of fruits to several abscission chemicals</p><p>varied considerably and the periods of low effectiveness coincided with higher and lower</p><p>indole-acetic acid and ABA levels, respectively, in the calyx abscission zone (Yuan et al.,</p><p>2001). These observations exemplify the role of endogenous auxins antagonizing or delaying</p><p>citrus fruit abscission, but as suggested above there are other instances showing inductive</p><p>effects of auxins on abscission. Thus, the postbloom fruit drop disease provoked by fungus</p><p>infection and characterized by premature fruit abscission has been associated with increases</p><p>of ethylene production and IAA and jasmonic acid (JA) amounts in the infected petals (Lahey</p><p>et al., 2004). Consistently, the application of both auxin transport and action inhibitors and JA</p><p>biosynthesis inhibitors after infection improved fruit retention suggesting an inductive role of</p><p>IAA and JA on young fruit abscission (Chen et al., 2006). These observations, apparently,</p><p>illustrate the dissimilar effects of auxins preventing and inducing abscission. It has also been</p><p>reported that treatments with methyl-jasmonate to mature citrus fruit are also able to induce</p><p>abscission (Hartmond et al., 2000).</p><p>Regulation of Fruit Set</p><p>The above evidence suggests that hormonal deficiencies, mostly reductions of GA levels</p><p>over the anthesis period, result in subsequent ovary and fruitlet drop. These effects are</p><p>apparent in both self-incompatible varieties such as ‘Clementine’ and in non-pollinated</p><p>ovaries of seeded cultivars. Consistently, GAs increase at anthesis while ABA is low shortly</p><p>thereafter in cultivars having low abscission rates (García-Papí and García-Martínez, 1984;</p><p>Talon et al., 1992). Again, the opposite can be found in self-incompatible species.</p><p>Furthermore, exogenous ABA increases ACC synthesis, ethylene production and abscission</p><p>in citrus fruit explants (Goren, 1993), whereas exogenous GAs suppress completely both</p><p>post-anthesis ABA increases and fruit abscission (Zacarias et al., 1995). Likewise, pollination</p><p>Citrus: An Overview of Fruiting Physiology</p><p>121</p><p>increases GA levels and reduces fruit abscission in seeded varieties, whereas emasculation</p><p>reduces the GA content and increases abscission. Once more, exogenous GAs suppress fruit</p><p>abscission of emasculated ovaries (Ben-Cheikh et al., 1997).</p><p>Taken together, it is concluded that GA deficiency is associated with ABA rise, ethylene</p><p>release and eventually ovary abscission (Figure 2). Interestingly, this hormonal sequence is</p><p>induced by other unfavorable conditions such as carbon shortage or water deficit also</p><p>provoking growth arrest and fruit abscission, as we will see below. Thus, a single hormonal</p><p>pathway triggering abscission appears to be induced through a variety of developmental and</p><p>environmental stimuli.</p><p>Figure 2. Regulation of citrus fruit abscission. Flower and ovary abscission through abscission zone A</p><p>(AZ-A), located between the branch and the peduncle. This abscission wave occurs at the beginning of</p><p>the fruit-set period and is negatively regulated by the endogenous levels of 3β-hydroxylated</p><p>gibberellins such as GA1 in ovaries. Fruitlet abscission during June drop occurs at the end of the fruit-</p><p>set period through AZ-C located in the calyx, in the interface between the floral disc and the ovary wall,</p><p>and is highly dependant on carbohydrate availability. Sugars in mature leaves are transported to</p><p>growing fruitlets and presumably inactivate AZ-C. Carbon shortage in fruitlets induces sequential</p><p>increases in abscisic acid. (ABA) and 1-aminocyclopropane-1-carboxylic acid. (ACC, the immediate</p><p>precursor of ethylene). This precursor is further oxidized to ethylene (C2H4) and the release of the gas</p><p>activates fruitlet abscission. In contrast to developing fruitlets, in mature ripe fruits sugar accumulation</p><p>might have an inductive role on the activation of pre-harvest abscission. It has also been suggested that</p><p>the balance between C2H4, acting as an accelerator of the process, and auxin, (AUX) acting as an</p><p>inhibitor, is one of the key factors regulating abscission of ripe fruit. In this model, AUX synthesized in</p><p>young leaves and transported to mature fruit operates as negative regulator of abscission protecting AZs</p><p>from high C2H4. The positive regulatory role of jasmonic acid. (JA) on fruit abscission is thought to be</p><p>mediated through C2H4 biosynthesis stimulation. The balance between AUX and ABA in mature fruits</p><p>may also be important in determining AZ-C sensitivity to the abscission stimulus. Arrows and T-shaped</p><p>lines indicate positive and negative regulation, respectively. From Iglesias et al. (2007) with permission</p><p>of Brazilian Society of Plant Physiology.</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>122</p><p>The observation that GAs are able to induce parthenocarpic fruit development in seeded</p><p>citrus is crucial to understand the GA role in fruit set. Thus, in seeded sweet orange,</p><p>parthenocarpic fruit development can be triggered by exogenous applications of gibberellins</p><p>benefit to the farmer is to be attained, crop performance must also</p><p>be evaluated under naturally changing tropical environmental conditions. After all, yield</p><p>improvement under such conditions is the major goal to be achieved.</p><p>REFERENCES</p><p>Alvim PT, Kozlowski TT, editors. Ecophysiology of tropical crops. New York: Academic</p><p>Press; 1977.</p><p>Boyer JS. Plant productivity and environment. Science 1982;218:443-8.</p><p>Chapple C, Campbell MM. Physiology and metabolism: Factors impacting plant productivity.</p><p>Trends Plant Sci. 2007;10:217-9.</p><p>DaMatta FM. Drought as a multidimensional stress affecting photosynthesis in tropical tree</p><p>crops. In: Hemantaranjan A, editor. Advances in plant physiology, Vol. 5. Jodhpur:</p><p>Scientific Publishers; 2003. p. 227-65.</p><p>DaMatta FM, Loos RA, Rodrigues R, Barros RS. Actual and potential photosynthetic rates of</p><p>tropical crop species. Braz. J. Plant Physiol. 2001;13:24-32.</p><p>Fábio M. DaMatta</p><p>6</p><p>El-Sharkawy MA, Cock JH. Photosynthesis of cassava (Manihot esculenta). Exp. Agric.</p><p>1990;26:325-40.</p><p>El-Sharkawy MA, de Tafur SM, Cadavid LF. Potential photosynthesis of cassava as affected</p><p>by growth conditions. Crop. Sci. 1992;32:1336-42.</p><p>Hallé F, Oldeman RAA, Tomlinson PB. Tropical trees and forests. Berlin: Springer-Verlag;</p><p>1978.</p><p>Janssens MJJ, Subramaniam B. Long-term perspective of fruit and other crops in the new</p><p>century. Acta Hort. 2000;531:23-7.</p><p>Kruger LC, Volin JC. Reexamining the empirical relation between plant growth and leaf</p><p>photosynthesis. Funct. Plant Biol. 2006;33:421-9.</p><p>Last FT, editor. Tree crop ecosystems. Amsterdam: Elsevier; 2001.</p><p>León J. Botánica de los cultivos tropicales. San José: Servicio Editorial IICA; 1987.</p><p>Long SP, Ainsworth EA, Leakey ADB, Nösberger J, Ort DR. Food for thought: lower-than-</p><p>expected crop yield stimulation with rising CO2 concentration. Science 2006;312:1918-</p><p>21.</p><p>Mish FC, editor. Merriam-Webster's collegiate dictionary. Springfield: Merriam Webster;</p><p>1993.</p><p>Salisbury FB, Ross CW. Plant physiology. Belmont: Wadsworth Publishing Co.; 1992.</p><p>Smith NJH, Williams JT, Plucknett DL, Talbot PT. Tropical forests and their crops. Ithaca:</p><p>Comstock Publishing Associates; 1992.</p><p>Wallace JS. Increasing agricultural water use efficiency to meet future food production.</p><p>Agric. Ecosyst. Environ. 2000;82:105-19.</p><p>In: Ecophysiology of Tropical Tree Crops ISBN 978-1-60876-392-4</p><p>Editor: Fabio DaMatta © 2010 Nova Science Publishers, Inc.</p><p>Chapter 2</p><p>BANANAS: ENVIRONMENT AND CROP PHYSIOLOGY</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>ABSTRACT</p><p>The bananas (Musa spp.) are thought to be particularly sensitive to changes in the</p><p>environment. This review considers some historical and recent investigations into the</p><p>response of the leaf, root and reproductive system to the environment. Monteith’s</p><p>analysis of the response of plants to intercepted radiation is appropriate for analyzing the</p><p>productivity of bananas and plantains. The banana is sensitive to soil water deficits, and</p><p>expanding tissues such as emerging leaves and growing fruit are among the first to be</p><p>affected. As soil begins to dry, stomata close and leaves remain highly hydrated, probably</p><p>through root pressure. Productivity is affected because of the early closure of stomata.</p><p>We find the common belief that bananas use large amounts of water does not have a</p><p>strong physiological basis. Improvements in water-use efficiency in irrigated plantations</p><p>could come from a closer match between plant water use and the amount of water</p><p>applied. We examine recent data on water-use efficiency of different banana cultivars and</p><p>propose that agronomists, physiologists and breeders could quantify the amount of water</p><p>available in each rain-fed environment and work towards directing more of that water</p><p>through the plant. The banana is day neutral for floral induction, but photoperiods of less</p><p>than 12 h are associated with a slowing in the rate of bunch initiation that is independent</p><p>of temperature expressed as growing degree days. This may contribute to seasonal</p><p>variations in banana flowering, even in more tropical environments with moderate</p><p>temperatures.</p><p>INTRODUCTION</p><p>People have been using bananas for at least 7,000 yr in Papua New Guinea (Denham et</p><p>al., 2003), possibly 6,000 yr in Uganda (Lejju et al., 2006) and 2,500 yr in Cameroon</p><p>(Mindzie et al., 2001). Today, most people of the world are familiar with this delicious fruit.</p><p>Edible clones of bananas and plantains, based on landraces, are derived from hybrids of the</p><p>wild sub-species of Musa acuminata Colla (A genome) and M. balbisiana Colla (B genome).</p><p>The wild bananas occur within the tropics from India to Oceania but there is a distinction</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>8</p><p>between the distribution of M. acuminata and M. balbisiana within that range. Musa</p><p>balbisiana overlaps the northern part of the range of M. acuminata and extends beyond it to</p><p>the west and north (Simmonds, 1962). The edible clones are now grown more widely</p><p>including in the subtropics of both hemispheres. Triploids (AAA, AAB and ABB) are most</p><p>common among the edible bananas with the plantains belonging to the AAB group. A special</p><p>feature of the edible clones is the parthenocarpic development of sterile fruit (Simmonds,</p><p>1959). The cultivars of the Cavendish sub-group (AAA) currently dominate the international</p><p>banana trade that is only 15% of the world’s annual production of 105 Mt (FAO, 2006). In</p><p>recent years, the world production of bananas has grown 3.3% annually. In countries such as</p><p>Brazil, a major producer, and Australia, a minor producer, bananas grow in tropical and</p><p>subtropical environments and on a wide range of soils.</p><p>Simmonds (1962) summarized the features of the wild bananas, based on observations in</p><p>the field, as being a group of broadly opportunistic plants that are intermediate in ecological</p><p>succession, distributed by animals, and requiring high temperature, humidity and light. They</p><p>do not tolerate competition or poor soil drainage and tend to be short-lived. Within the wild</p><p>bananas, Simmonds noted significant differences between species in their ecological demands</p><p>and tolerances. Early comments about bananas, particularly on the cv. ‘Gros Michel’ (AAA</p><p>group) used by the international trade early in the 20th century, focus on the sensitivity of the</p><p>plant to changes in the environment (Popenoe, 1941). Most of the research on the effect of</p><p>environment on Musa species has been on members of the edible bananas. There is a need to</p><p>know more about the responses of the wild species that provide the genetic basis for the</p><p>edible genotypes.</p><p>LEAF SYSTEM</p><p>The banana is a monocotyledon with an underground main axis that is a sympodium and</p><p>is commonly called a ‘corm’ (see Figure 1). The corm supports a series of leaves the sheaths</p><p>of which form the ‘pseudostem’. The leaves arise in sequence from the apex of each</p><p>vegetative shoot. A lateral shoot (sucker), if removed from the parent plant and transplanted,</p><p>begins a new individual mat. In ratoon plants (suckers arising from, and remaining attached</p><p>to, a parent) the first leaves on the shoot are scale like, subsequent leaves are lanceolate, and</p><p>later in development laminate leaves are produced. The petiole is an extension of the sheath</p><p>and this leads to the midrib that supports the lamina. In total, 30 to 50 or more leaves may be</p><p>produced on a shoot but at any one time only 10 to 14 living leaves are present external to the</p><p>pseudostem. As each leaf develops within the pseudostem the lamina increases in area until it</p><p>begins to emerge from the top of the pseudostem. It may take 7 to 14 d for one leaf to emerge.</p><p>During that time, increase in area ceases for those parts of the lamina that have emerged. Each</p><p>laminate leaf is larger than its predecessor except for the last couple of leaves that emerge</p><p>before the inflorescence. These leaves are smaller in area</p><p>to emasculated and unfertilized gynoecia. This exogenous supply is thought to substitute the</p><p>endogenous hormones normally provided by the seeds. Fruit treated with GA set and</p><p>elongated as much as pollinated fruit during the first phase of growth just until June drop.</p><p>However, none of these GA treated parthenocarpic fruit overcame June drop and came close</p><p>to reach maturation and ripening (Ben-Cheikh et al., 1997) suggesting that although GA may</p><p>counteract the failure in the hormonal signaling during the first phase of growth, other pivotal</p><p>factors in seeded varieties are required during June drop and thereafter. Hence, exogenous</p><p>GAs set fruit and trigger initial seedless fruit development in both “facultative” and “truly”</p><p>parthenocarpic varieties although only in facultative cultivars is fruit growth fully completed</p><p>until ripening. These observations indicate both that GAs are pivotal factors controlling initial</p><p>fruit set and that other components are also essential during June drop.</p><p>The Role of Carbohydrates</p><p>After hormonal induction of fruit growth, nutrients may have regulatory functions on</p><p>their own and/or through the maintenance of adequate hormonal levels (Gillaspy et al., 1993).</p><p>The average number of flowers produced in a normal citrus tree is by far extremely high in</p><p>comparison with the number of fruits that the same tree can support until ripening. Hence,</p><p>many fruits are abscised during growth apparently due to competition for nutrients especially</p><p>photoassimilates. During the initial moments of phase I, citrus fruitlets function as</p><p>carbohydrate utilization sinks but over the final stages of this period and during the transition</p><p>from cell division to cell enlargement, developing fruits shift their metabolism and start to</p><p>behave as storage sinks (Mehouachi et al., 1995). Interestingly, defoliation during phase I,</p><p>that reduces carbohydrate amounts, arrests fruitlet growth and promotes massive abscission</p><p>(Mehouachi et al., 1995, 2000) whereas defoliation after the June drop also arrests growth but</p><p>does not induce abscission (Lenz, 1967).</p><p>The link between carbohydrates and fruit growth is currently supported by a wide body of</p><p>evidence including several studies on source-sink imbalances, defoliation, girdling, shading,</p><p>sucrose supplementation, defruiting and fruit thinning (Goldschmidt and Koch, 1996; Iglesias</p><p>et al., 2003; Syvertsen et al., 2003). First, the enhancement of carbohydrate availability was</p><p>associated with an improvement of fruit set and yield of citrus trees (Goldschmidt, 1999).</p><p>Later, a strong relationship was demonstrated between carbohydrate levels available to</p><p>fruitlets and the probability of abscission (Gómez-Cadenas et al., 2000; Iglesias et al., 2003).</p><p>This phenomenon that has also been described for other tree species is also supported by</p><p>studies on translocation of 14C metabolites and CO2-enrichment experiments (Moss et al.,</p><p>1972; Downton et al., 1987). Hence, photosynthesis activity has been proved to be crucial</p><p>since high carbohydrate requirements during fruit set increases photosynthetic rate (Iglesias et</p><p>al., 2002). This suggestion also implies that a reduction in net CO2 assimilation rate results in</p><p>lower sugar production and fruit set. Moreover, in this study it was proposed that sugar</p><p>concentration in leaves might be the signal that regulates the feed-back mechanism</p><p>stimulating photosynthesis in response to fruit sugar demand. Thus, once carbon demands are</p><p>fulfilled, carbohydrate accumulation may elicit end-product feedback control of</p><p>Citrus: An Overview of Fruiting Physiology</p><p>123</p><p>photosynthesis. For example, it is known that ringing that generally increases fruit set and</p><p>carbon availability (Iglesias et al., 2006b) probably because of the transitory block of phloem</p><p>flux transport (Wallerstein et al., 1978; Yamanishi, 1995) also represses total photosynthetic</p><p>activity (Iglesias et al., 2002). Indeed, girdling decreases photosynthesis in the bulk of</p><p>developing vegetative shoots but stimulates it in leafy fruiting shoots (Rivas et al., 2007). An</p><p>additional interesting observation relies on the fact that the positive effect of both pollination</p><p>and exogenous GAs on fruit set and growth may also partially operate through the induction</p><p>of a stronger mobilization of 14C metabolites to ovaries (Powell and Krezdorn, 1977).</p><p>Furthermore, exogenous GAs have also been shown to stimulate growth and increase carbon</p><p>supply in vegetative tissues (Mehouachi et al., 1996). Collectively all this information indicates</p><p>that sugars are deeply implicated in the regulation of fruitlet growth and that overall carbon</p><p>deficiency induces fruit abscission.</p><p>Regulation of June Drop</p><p>Although the specific mechanism involved in the response of fruit growth to</p><p>carbohydrates has not been studied at the molecular level many observations suggest that</p><p>sugars may act not only as essential nutrient factors but also as signals triggering specific</p><p>hormonal responses (see, for example, Zhou et al., 1998; Roitsch, 1999). As above, the</p><p>essential observation linking carbohydrate and abscission was the finding that carbon</p><p>shortage during ovary and fruitlet drop increased ABA and ethylene and that both are</p><p>involved in the induction of early abscission (Gómez-Cadenas et al., 2000). This information</p><p>was provided by defoliation treatments that in citrus do not change the water status of the</p><p>developing fruits but do alter considerably the nutrient supply (Mehouachi et al., 1995). The</p><p>alterations in the nutrient balance that are accompanied with increased fruitlet abscission</p><p>during the June drop provoke an unambiguous tendency to both increase nitrogen content and</p><p>to reduce carbon shortage. Interestingly, abscission intensity correlated positively with</p><p>carbohydrate shortage and later it was also demonstrated that the increases in the abscission</p><p>rates induced by different defoliation treatments paralleled ABA and ACC levels detected in</p><p>the abscinding fruitlets (Gómez-Cadenas et al., 2000). The simplest interpretation of these</p><p>observations suggests that ABA acts as a sensor of the intensity of the nutrient shortage</p><p>modulating the levels of ACC and ethylene, the final activator of abscission. Manipulative</p><p>experiments of the amounts of endogenous hormones also led to the conclusion that, although</p><p>the ABA rise precedes the ACC increase, both are certainly required for fruit abscission.</p><p>Thus, two main conclusions can be extracted from these observations: first, that the fruit fall</p><p>that takes place during June drop is very likely due to the carbohydrate insufficiency caused</p><p>by an increased carbon demand of a huge population of expanding fruitlets; and second,</p><p>carbon deficiency is again associated with ABA rise, ethylene release and massive fruitlet</p><p>abscission (Figure 3), that is, with the hormonal sequence suggested to operate in developing</p><p>reproductive structures during early ovary to fruitlet transition (see above) and also during water</p><p>stress-induced abscission (see below).Interestingly, this hormonal abscission pathway appears to</p><p>be induced through a variety of developmental and environmental stimuli.</p><p>This idea that citrus fruit abscission is connected to carbohydrate availability was initially</p><p>anticipated by Goldschmidt and Monselise (1977) who suggested that citrus might possess an</p><p>internal self-regulatory mechanism that adjusts fruit load to the ability of the tree to supply</p><p>Domingo J. Iglesias, Manuel Cercós, José M. Colmenero-Flores et al.</p><p>124</p><p>metabolites. The above findings identify leaf sugar content, ABA and ethylene as major</p><p>components of the self-regulatory adjusting mechanism visualized by those authors. The</p><p>proposed hormonal sequence also offers a plausible explanation for the naturally occurring</p><p>abscission and physiological bases for the photoassimilate competition hypothesis.</p><p>Figure 3. Regulation of citrus fruit set and growth. Aside from flowering, other major regulating factors</p><p>than their predecessors.</p><p>The maximum amount of leaf area on a shoot coincides with the emergence of the bunch</p><p>(inflorescence) from the top of the pseudostem. After this, no new leaves are produced on that</p><p>shoot because the bunch is terminal and the leaf area then begins to decline over time as the</p><p>older leaves senesce. During the development of a single shoot, lateral shoots or suckers</p><p>develop from buds on the corm and these begin to grow, each producing their own sequence</p><p>Bananas: Environment and Crop Physiology</p><p>9</p><p>of leaves and an inflorescence. In commercial plantations, most suckers are removed to allow</p><p>a single shoot to develop on each plant. The capacity of a canopy of leaves in a plantation to</p><p>intercept light and fix carbon is measured by the leaf area index (LAI). The LAI includes the</p><p>area of all green leaves on all shoots present. It is the area of leaf (single side) divided by the</p><p>area of land occupied by the plants. It varies with location, planting density and a number of</p><p>other factors, including season, and ranges from 2 to 5. This is not large compared with an</p><p>apple tree that may have an LAI of 7 or more (Proctor et al., 1976), but even apple trees</p><p>normally have LAI within the range of 3.5 to 4.6 when the leaves are fully grown (Jackson,</p><p>2003). The individual leaves on bananas can be quite large, up to 2 m2, and this gives the</p><p>impression that LAI must be high, compared with other crops, but measurements suggest this</p><p>is not the case. In a banana plantation with LAI of 4.5, about 90% of the ground will be</p><p>shaded at noon on a sunny day. This implies that about 90% of the incoming radiation is</p><p>being intercepted by the leaf canopy. Thus increasing LAI beyond this value is of little benefit</p><p>to the plantation because most of the incoming radiation is already being intercepted.</p><p>Figure 1. ‘Cavendish’ cultivars in plantations provide much of our knowledge of banana physiology but</p><p>most bananas and plantains are genotypes other than ‘Cavendish’ and grow in complex environments -</p><p>a challenge! Photo by the author.</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>10</p><p>Interception of Radiation, Photosynthesis and Productivity</p><p>Leaves intercept radiant energy from the sun and use it to fix carbon dioxide and</p><p>synthesize carbohydrates that are used for plant function and growth. Several authors have</p><p>reported measurements of the relationship between light received and the rate of net CO2</p><p>assimilation (A) of individual leaves in banana. These data were summarized by Turner</p><p>(1998a, 1998b). There is considerable variation in the form of light response curves between</p><p>experiments, cultivars and environmental conditions. The maximum rate of A may vary from</p><p>5 to 25 μmol CO2 m-2s-1, and the saturation value for the photosynthetic photon flux density,</p><p>may vary from 700 to more than 2,000 μmol photons m-2 s-1. The experiments of Robinson et</p><p>al. (1992) show that A is increased by the presence of growing organs on the plant. This may</p><p>be a reason why Thomas and Turner (2001) found that A of leaves on rapidly growing</p><p>vegetative plants of cv ‘Williams’ (AAA, Cavendish subgroup) did not reach light saturation,</p><p>even at full sunlight. There is a need to use the data available on light response curves to</p><p>simulate carbon fixation by a canopy of banana leaves. In this way the significance of</p><p>differences in the light response curve for functioning of the canopy could be evaluated. One</p><p>may expect that while an individual leaf saturates for photosynthetic photon flux density, a</p><p>canopy does not and so the primary production (CO2 fixed per unit ground area) of a canopy</p><p>tends to increase the more light it receives (Jones, 1992). This analysis assumes the canopy</p><p>cover is complete. Furthermore, if LAI is low (< 3) then the light saturation of all leaves in</p><p>the canopy is more likely to be reached and the canopy will show saturation for light</p><p>(Thornley and Johnson, 2000). Banana leaves behave somewhat differently since they are</p><p>able to fold as incoming net radiation increases. Folding reduces the radiant energy being</p><p>intercepted by the folded lamina and increases the probability that the leaf will be operating at</p><p>less than light saturation. Lamina folding sheds radiation to the lower leaves if LAI is high, or</p><p>to the ground if LAI is low.</p><p>The relationship between leaf A and its intercellular CO2 concentration (Ci) can give</p><p>clues about the factors limiting photosynthesis. Sharkey et al. (2007a, 2007b) proposed a</p><p>curve fitting procedure for analyzing A/Ci curves. Schaffer et al. (1996) measured the effect</p><p>of root restriction and high ambient CO2 concentration on the A/Ci response of leaves of cv.</p><p>‘Gros Michel’ (AAA group). We subjected their published data to the curve fitting procedure</p><p>of Sharkey et al. (2007b) which has five outputs: the maximum carboxylation rate allowed by</p><p>Rubisco (Vcmax); the rate of photosynthetic electron transport (J); triose phosphate use (TPU);</p><p>day respiration rate (Rd); and mesophyll conductance (gm). The procedure standardizes the</p><p>values of these parameters to 25˚C to allow comparison across experiments. Root restriction</p><p>reduced plant growth by 25% and it affected the biochemistry of photosynthesis by reducing</p><p>Vcmax 46% and increasing Rd by 44% (Table 1). The changes in J, TPU and gm were smaller in</p><p>magnitude. Increasing ambient CO2 concentration from 350 to 1,000 μL L-1 more than</p><p>doubled plant growth and it changed the biochemistry of photosynthesis. It reduced Vcmax by</p><p>more than half and increased Rd fivefold (Table 1). There were smaller effects on J, TPU and</p><p>gm. This analysis of the data of Schaffer et al. (1996) complements their findings and</p><p>quantifies the five parameters of the A/Ci curves.</p><p>At the level of the crop, two approaches have been used to analyze the response of</p><p>bananas to incoming solar radiation. The first approach includes experiments to determine the</p><p>effect of shading on productivity. This is sensible to investigate because increasing plant</p><p>Bananas: Environment and Crop Physiology</p><p>11</p><p>density reduces the amount of sunlight available per plant and in gardens bananas may be</p><p>grown as an understory. Turner (1998b) summarized the findings of shading experiments and</p><p>these show that in deep shade, the increase in yield is proportional to the increased amount of</p><p>light received. At higher levels of radiation, other factors begin to limit yield and so yield</p><p>remains the same despite increased radiation (Figure 2). The second approach is that proposed</p><p>by Monteith (1981) where, for plants in general, the amount of growth is proportional to the</p><p>intercepted radiation, irrespective of the amount of incoming radiation. This approach has</p><p>been widely accepted among crop physiologists and in bananas has been used to estimate the</p><p>seasonal demand for nitrogen (Turner, 1990), the productivity of bananas in a range of</p><p>environments (Turner, 1998b) and forms the basis of the growth module in the SIMBA model</p><p>of a banana crop system developed by Tixier et al. (2008). The equation of Monteith has been</p><p>modified for bananas to include the effects of temperature and plant vigor, expressed as the</p><p>cycling time of ratoon crops (Turner, 1994, 1998b). Data are needed to determine the</p><p>coefficients, especially the radiation use efficiency. It is possible using this approach to</p><p>estimate the potential yield for a site (Turner, 1998b) and, despite the number of assumptions</p><p>this is a good base for further discussions about what factors might be limiting yield in a</p><p>given situation.</p><p>Table 1. The parameters of the photosynthetic carbon dioxide response curve for</p><p>banana cv. ‘Gros Michel’ (AAA group). The A/Ci response curves come from the</p><p>experiments of Schaffer et al. (1996) who applied treatments of root restriction</p><p>(container volume, 20 or 200 L) and ambient CO2 concentration (350 or 1,000 ppm</p><p>CO2). The A/Ci parameters were derived from the curve fitting procedure of Sharkey et</p><p>al. (2007b). Vcmax,</p><p>maximum carboxylation rate allowed by Rubisco; J, rate of</p><p>photosynthetic electron transport; TPU, triose phosphate use; Rd, day respiration; and</p><p>gm, mesophyll conductance. From Turner et al. (2007) with permission of Brazilian</p><p>Society of Plant Physiology</p><p>Parameter Treatments</p><p>Units 20 L pot 200 L pot 350 CO2 1,000 CO2</p><p>Vcmax μmol m-2s-1 539 996 1249 539</p><p>J μmol m-2s-1 268 290 252 296</p><p>TPU μmol m-2s-1 19.1 20.6 18.0 20.9</p><p>Rd μmol m-2s-1 13.9 9.6 3.4 17.7</p><p>gm μmol m-2</p><p>s-1 Pa-1</p><p>1.21 1.14 1.22 0.91</p><p>Total plant</p><p>dry weight</p><p>g 1,686 2,272* 1,142 2,731*</p><p>*container volume and ambient CO2 concentration both significantly affected total plant dry weight (P</p><p>≤ 0.05).</p><p>Monteith’s approach gives insights into the effect of protected cultivation on banana</p><p>yield. In that situation there is an increase in productivity (20-30%) but a reduction in the</p><p>amount of solar radiation (20%) beneath the protective cover (Galan Sauco et al., 1992). The</p><p>model in Figure 2 would indicate that such a reduction in incoming radiation would either</p><p>reduce yield or have no impact. Monteith’s model accounts for the observed response because</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>12</p><p>protected cultivation increases LAI and changes the extinction coefficient such that the plants</p><p>intercept more incoming radiation than their counterparts growing in an open plantation</p><p>(Turner, 1998b). The plants in the open do not have enough leaf area to intercept as much</p><p>radiation as their counterparts under cover, and the arrangement of their leaves magnifies this</p><p>effect.</p><p>Proportion of sunlight, %</p><p>0 20 40 60 80 100</p><p>Y</p><p>ie</p><p>ld</p><p>, %</p><p>o</p><p>f m</p><p>ax</p><p>im</p><p>um</p><p>0</p><p>20</p><p>40</p><p>60</p><p>80</p><p>100</p><p>A</p><p>B</p><p>C</p><p>Figure 2. A schematic diagram of the response of banana yield to shade. Line A is the expected</p><p>response of yield to increased light based on the efficiency of growth of well-shaded plants. Lines B</p><p>and C show the response to increased light when factors other than light now limit yield above 20% or</p><p>50% light, respectively. From Turner et al. (2007) with permission of Brazilian Society of Plant</p><p>Physiology.</p><p>Water Relations of the Bananas</p><p>Knowledge of the water relations of a plant, particularly its leaves, has long been based</p><p>on understanding the physiological responses of the plant to soil and atmospheric water</p><p>deficits. This knowledge can assist in management decisions concerning irrigation, water use</p><p>and productivity. While extensive gains in our knowledge of plant responses have been</p><p>achieved for many plants, the unique morphology and anatomy of bananas has hindered the</p><p>rate of achievement. Water relations of plant tissues are described using changes in volume</p><p>(usually the amount of water present, since water is incompressible) and changes in the</p><p>thermodynamic status of the water in the tissues. In bananas it is the presence of large air</p><p>pockets within the leaves, and laticifers containing latex within the leaves, fruit and corm that</p><p>hinders the use of standard methods of measuring water relations. In banana leaves it is</p><p>thought these air pockets could fill when volumetric methods of measuring water status are</p><p>used (Kallarackal et al., 1990), especially when leaf tissues are being rehydrated. Exuding</p><p>latex makes it difficult to distinguish water exuding from xylem when using the standard</p><p>pressure chamber for measurements of leaf water potential (Ψw). The laticifers in the lamina</p><p>Bananas: Environment and Crop Physiology</p><p>13</p><p>are several centimeters long and those in the midrib and leaf sheath can be several meters</p><p>long. The laticifers contain fluids at a lower Ψw than the surrounding tissues and this is why</p><p>when banana leaves or fruit are cut, the contents of the laticifers exude as they are replaced by</p><p>water from the surrounding tissues. If no latex exudes on cutting, then the leaf could be</p><p>experiencing a water deficit.</p><p>Despite these challenges of anatomy and morphology, water relations of bananas have</p><p>been measured using both volumetric and thermodynamic methods. Additionally the extent of</p><p>leaf folding has been used. Each of the thermodynamic, volumetric or morphological</p><p>techniques has its strengths and weaknesses and can indicate different aspects of the water</p><p>status of leaf tissues. Early studies that assess leaf water status in bananas used mainly</p><p>volumetric methods such as leaf water content (g H2O g-1 leaf DM), specific leaf water</p><p>content (g H2O m-2 leaf surface) (Shmueli, 1953; Chen, 1971) or relative leaf water content</p><p>(Turner and Lahav, 1983). These studies typically show large responses in plant behavior</p><p>within a very narrow and high (moist) range of values of leaf water status measured by these</p><p>techniques. In a later study Turner and Thomas (1998) confirmed this finding and showed air</p><p>spaces within the leaf were not biasing volumetric measurements. In fact the high values for</p><p>volumetric techniques (relative water content) indicate water does not fill the air spaces and</p><p>furthermore, in banana, high vacuum is needed to fill these air spaces with water (Turner and</p><p>Thomas, 1998). Volumetric measurements of leaf water status indicate that banana plants</p><p>remain hydrated even when showing other signs of water deficit.</p><p>Methods of measuring the thermodynamic status of leaf water, such as with a pressure</p><p>chamber, have been used for bananas (Hegde and Srinivas, 1989; Thomas and Turner, 1998).</p><p>Milburn et al. (1990) developed a technique to measure plant water status based on the</p><p>osmotic potential of exuding latex. This technique avoids the dangers of differentiating xylem</p><p>water, which has to be forced from the leaf, and latex fluid that exudes freely from severed</p><p>leaves. Despite a lack of similarity in Ψw measured by the latex based method and xylem</p><p>water based measurements both methods showed declining leaf water status in droughted</p><p>plants which could be linked to other plant functions (Hedge and Srinivas, 1989; Kallarackal</p><p>et al., 1990). This contrasts with the findings of Thomas and Turner (1998) and Turner and</p><p>Thomas (1998) who showed measurements of leaf Ψw using either the exuding xylem or</p><p>relative leaf water content could not be reliably linked to plant functions such as stomatal</p><p>aperture, net photosynthesis or leaf folding. Leaf Ψw measured by the exuding latex method</p><p>appeared the best for determining leaf water status, but even this shows a small change in</p><p>plants experiencing soil water deficit (Thomas and Turner, 1998; Turner and Thomas, 1998)</p><p>supporting the hydrated status of banana leaves although the soil is dry.</p><p>The laminae of banana leaves fold in response to environmental stimuli. This movement</p><p>does not reflect wilting of the leaf because if the leaf is excised and inverted, the laminae do</p><p>not flop apart. Lamina folding is due to differential turgor of cells within the pulvinar bands</p><p>caused by water movement accompanying ion movements (Satter, 1979; W. Robertson,</p><p>unpublished data). The folding of banana leaves typically follows a diurnal rhythm with the</p><p>leaves more horizontal during the night, and early morning, becoming more vertical during</p><p>periods of bright sunlight, and returning to more horizontal positions in late afternoon. These</p><p>changes in turgor within the cells of the pulvinar bands are similar to changes in stomatal</p><p>aperture that is controlled by the turgor of guard cells. In addition, the laminae of banana</p><p>leaves fold in response to soil drought (Milburn et al., 1990; Thomas and Turner, 1998;</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>14</p><p>Turner and Thomas, 1998) suggesting leaf folding may reflect leaf water status, albeit</p><p>somewhat unreliably. However, Lu et al. (2002) did not find any link between leaf folding</p><p>and soil water deficit. Lu et al. (2002) measured water use of banana plants using a sap flow</p><p>system calibrated against gravimetrically determined water loss. This system measured water</p><p>use by insertion of heat sensing probes into the central cylinder of the banana corm through</p><p>which water flows from the root system to the shoot. It is a widely used technique to measure</p><p>water use of trees, and has the advantage over other systems that measure whole plant water</p><p>use in that the water sensing unit (typically heat based) is localized thus causing less damage</p><p>to the plant being measured and hence greater reliability of data. Alternate systems can</p><p>overheat and greatly damage or kill banana plants thus rendering measurements useless (D.S.</p><p>Thomas, unpublished data).</p><p>Despite our best efforts, there is not a straightforward link between leaf scale gas</p><p>exchange and leaf water status in bananas. Often, turgor-based changes within leaves such as</p><p>changes in stomatal aperture, leaf folding or leaf elongation in response to soil water deficit or</p><p>to high vapor pressure deficit (VPD) do not correspond with changes in leaf water status</p><p>measured by classical methods based on either thermodynamics or volumetric water content.</p><p>On first thoughts this is a concern as it indicates our knowledge is not complete. However,</p><p>hypotheses to explain these relationships can be developed.</p><p>Stomatal aperture, which greatly influences net photosynthesis through its effect on the</p><p>diffusion of CO2 into the leaf and its more tenuous link to productivity, is controlled by turgor</p><p>of the guard cells. It is possible for the turgor of guard cells to operate reasonably</p><p>independently of the water relations of the plant or bulk leaf. Extreme examples include</p><p>stomatal responses to light or concentration of CO2, but stomata also respond to the amount</p><p>of water vapor in the air, in addition to more classical ‘within plant’ controls such as leaf Ψw</p><p>or changes in plant growth regulators such as abscisic acid. Localized water loss from the</p><p>stomatal region is thought to be the mechanism by which stomata respond to VPD. This</p><p>creates a gradient in Ψw between the guard cells and stomatal subsidiary cells and affects</p><p>guard cell turgor. If stomata respond directly to VPD it becomes clear why the relationship</p><p>between stomatal aperture and bulk leaf water status is variable (Schulze et al., 1972; Turner</p><p>et al., 1985). A decrease in stomatal aperture and/or stomatal conductance (gs) will reduce</p><p>leaf transpiration but should not decrease water flow to the leaf from the plant and soil,</p><p>therefore the net water balance of the leaf should increase. Models of the response of stomata</p><p>to VPD suggest that guard cells are at or near the end of the Ψw gradient and thus a change in</p><p>leaf Ψw is likely to affect the guard cells to a greater extent than the remainder of the leaf</p><p>(Shackel and Brinckmann, 1985). This means guard cells will close even if the leaf is</p><p>hydrated. The findings of Thomas et al. (1998) in banana (cv. ‘Grand Nain’, AAA, Cavendish</p><p>subgroup) and Thomas and Eamus (1999) in tropical eucalypts that leaf transpiration can</p><p>decline in direct response to low humidity supports the idea that leaf water status can increase</p><p>and leaves appear well hydrated when stomatal aperture is independently restricted by these</p><p>same environmental conditions. Additionally the observations of Thomas and Turner (1998)</p><p>and Turner and Thomas (1998) that stomatal responses can be independent of plant water</p><p>status can be explained by this mechanism. The independent measurements of whole plant</p><p>water use using sap flow technology (Lu et al., 2002) show plant water use follows a diurnal</p><p>pattern with greater water use in sunnier conditions and periods of higher VPD. This is</p><p>consistent with earlier reports of patterns of gs measured on small leaf sections. The “feed-</p><p>Bananas: Environment and Crop Physiology</p><p>15</p><p>forward” response of stomata to humidity described above is not mutually exclusive from the</p><p>feed-back response to low leaf Ψw /low plant hydration. Both mechanisms could be operating</p><p>in unison to maintain a hydrated leaf, yet one where stomatal aperture and water loss are</p><p>controlled by soil, plant and atmospheric water content.</p><p>The Use of Water</p><p>There is a conundrum in our knowledge of the link between water and productivity in</p><p>bananas. Anecdotal evidence, based on experience in plantations, supports the view that</p><p>bananas require “abundant and constant supplies of water” (Popenoe, 1941). On the other</p><p>hand, physiological investigations suggest that bananas are remarkably tolerant of soil water</p><p>deficit (Kallarackal et al., 1990) and can evaporate less water than other crops (Lu et al.,</p><p>2002).</p><p>The notion that bananas require abundant and constant supplies of water is supported</p><p>experimentally by numerous investigations into the water use of bananas and their response to</p><p>irrigation in a range of environments in the tropics (Meyer and Schoch, 1976; Meyer, 1980;</p><p>Holder and Gumbs, 1983; Hegde and Srivinas, 1989) and subtropics (Kebby and Eady, 1956;</p><p>Trochoulias, 1973; Lahav and Kalmar, 1981; Robinson and Alberts, 1986, 1987). Robinson</p><p>(1996) summarizes these and other observations by pointing to the high sensitivity of banana</p><p>to soil water deficit and that in practice, the “little and often” approach to scheduling</p><p>irrigation is the best strategy, in addition to the large amount of water that is needed for high</p><p>production.</p><p>So, why might investigations into the physiology of the plant suggest a different</p><p>outcome, that banana plants do not use a lot of water and that they might be quite hardy? To</p><p>explain the need for large amounts of water to be applied as irrigation, several features of the</p><p>banana plant have been highlighted over a number of years and are widely believed (van</p><p>Vosselen et al., 2005; Opfergelt et al., 2006). Robinson (1996) summarized these features: (i)</p><p>a high potential for transpiration because of the large, broad leaves and a high LAI; (ii)</p><p>shallow roots in comparison with other fruit crops; (iii) a poor ability to withdraw water from</p><p>drying soil; and (iv) a rapid physiological response to soil water deficit. Nonetheless, what</p><p>physiological evidence exists to support these features? Large, broad leaves do not mean a</p><p>high rate of transpiration per unit of leaf area. Water vapor moves from inside to the outside</p><p>of the leaf in the direction of the leaf-to-air vapor pressure difference. Water vapor diffuses</p><p>through the stomata and the leaf boundary layer, which is the layer of unstirred air adjacent to</p><p>the leaf surface, before it reaches the atmosphere. Low wind speed and large leaf area</p><p>increase the depth of the boundary layer, slowing the movement of water vapor from the leaf</p><p>to the air. Thus, all things being equal, we could expect less evaporation per unit of leaf area</p><p>from large leaves than small leaves. In reality the situation is more complex because sensible</p><p>heat also diffuses across the boundary layer. Thus large leaves will be warmer than smaller</p><p>leaves, as demonstrated clearly by Taylor and Sexton (1972). An increase in wind speed will</p><p>reduce the boundary layer thickness, cool the leaf and consequently reduce the leaf-to-air</p><p>vapor pressure difference, which drives evaporation from the leaf. The reduced gradient and</p><p>the thinner boundary layer will both influence evaporation rate but will operate in different</p><p>directions, making the prediction of water loss from the leaf difficult to generalize. A feature</p><p>of banana leaves is their ability to “‘shed” solar radiation by folding the lamina downwards</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>16</p><p>(Thomas and Turner, 2001). In dense plantations this allows more radiation into the lower</p><p>leaf layers and distributes the intercepted radiation more evenly across the canopy. Where</p><p>LAI is low, the effect is to allow more radiation to reach the ground. In addition, under the</p><p>influence of wind, the laminae tear into strips, making the leaves ‘smaller’ and the</p><p>experiments of Eckstein et al. (1996) show that this changes the physiology of the leaves.</p><p>Transpiration from sections of leaves is often measured with a gas analysis system where</p><p>a small section of leaf is enclosed in a chamber</p><p>through which there is a flow of air (Robinson</p><p>and Bower, 1986; Schaffer et al., 1996; Thomas and Turner, 2001). The boundary layer in the</p><p>chamber is determined by the flow rate of the air stream and the size of the chamber. It is</p><p>standardized so that gs can be estimated. The boundary layer in these chambers is very</p><p>different in magnitude to that encompassing a whole leaf that influences evaporation from the</p><p>whole leaf or plant. Lu et al. (2002) measured the water use of whole banana plants cv.</p><p>‘Williams’ (AAA, Cavendish subgroup) by using gravimetric and sap flow techniques. Water</p><p>flowing from the root system to the leaves must flow through the corm and sap flow sensors</p><p>placed there can give an estimation of the water use by the whole plant. In this case the</p><p>boundary layer of the leaves is not modified by the instrumentation used to measure</p><p>transpiration, such as it is when a gas exchange system is used. Lu et al. (2002) compared the</p><p>maximum sap flux density of 15 g cm-2 h-1 that they measured in the corm of banana plants</p><p>with published values for spruce (19 g cm-2 h-1), mango (35 g cm-2 h-1) and tropical rainforest</p><p>tree species (40 g cm-2 h-1). They pointed out that the value for banana was lower than for</p><p>other species and they attributed this to the low leaf area/sapwood area ratio in banana</p><p>compared with other species. Thus large leaves can be misleading as banana has large leaves</p><p>but the sap flux density in the corm is less than that measured for tree species with small</p><p>individual leaves.</p><p>A canopy with a high LAI could be expected to evaporate more water than a canopy with</p><p>lower LAI. In the longer term, the amount of water evaporated from a leaf canopy will be</p><p>proportional to the amount of radiation intercepted because energy is needed to convert water</p><p>from a liquid to vapor. About 90% of the incoming radiant energy is intercepted at an LAI of</p><p>4.5 to 5.0 for bananas, although under protected cultivation this may reach 94% (Tanny et al.,</p><p>2006). Thus LAI beyond about 5.0 is unlikely to contribute greatly to increased evaporation.</p><p>As we have already seen, the LAI of banana plantations is similar to that of other fruit crops.</p><p>The impact of a shallow root system is to reduce the amount of water available to the</p><p>crop. Robinson (1995) summarized a number of studies of soil water extraction by bananas</p><p>and concluded that for irrigation purposes, the effective rooting depth falls in the range of 0.3</p><p>to 0.4 m, which could be regarded as shallow. However, there are instances where banana</p><p>plants (cv. ‘Valery’, AAA, Cavendish subgroup) growing in clay soils have not responded to</p><p>irrigation (Madramootoo and Jutras, 1984) and in this case it was thought that the dry-land</p><p>plants were able to obtain water from below 0.3 m depth. The root system is strongly</p><p>modified by the soil environment. Popenoe (1941) thought that oxygen supply, related to soil</p><p>texture, was a major factor in determining the depth of the root system of cv. ‘Gros Michel’</p><p>(AAA), with shallow root systems reflecting a reduced supply of oxygen at depth. In deep</p><p>soils roots of bananas can be found down to 1.5 to 1.8 m. More recently, Lecompte et al.</p><p>(2002) found that the mean angle of exit of roots from the corm of cv. ‘Grand Naine’ (AAA,</p><p>Cavendish subgroup) was 30˚. This would mean that at 1 m from the corm many roots should</p><p>reach 0.58 m depth, considerably further than the 0.3 to 0.4 m that is a working depth for</p><p>irrigation. The “shallow” nature of banana root systems may be more a reflection of edaphic</p><p>Bananas: Environment and Crop Physiology</p><p>17</p><p>factors than an inherent feature of the crop. Whatever the reason for the shallow root system,</p><p>this needs to be taken into account when applying irrigation.</p><p>The capacity of banana roots to withdraw water from drying soil has not been evaluated,</p><p>to our knowledge. The issues here are the gradient in Ψw between the soil at the root surface</p><p>and the stele and the capacity of the root to conduct water across the cortex to the stele. The</p><p>hydraulic conductivity of banana roots cv. ‘Williams’ (AAA, Cavendish subgroup), when</p><p>well supplied with water, is somewhat higher but of the same order of magnitude as that of</p><p>maize (Gibbs et al., 1998; Aguilar et al., 2003) and so is not unique. Root hydraulic</p><p>conductivity may fall as soil dries, as is the case for many plants, but this situation is not</p><p>universal (Bramley et al., 2007). The magnitude and significance of changes in root hydraulic</p><p>conductivity in bananas has yet to be established.</p><p>For water to flow into roots, Ψw in the root needs to be less (more negative) than that in</p><p>the soil. Several investigations have shown that banana leaves remain quite hydrated as soil</p><p>dries (Shmueli, 1953; Kallarackal et al., 1990; Turner and Thomas, 1998). Leaf Ψw as high as</p><p>-0.1 to -0.5 MPa occurs in banana plants cv. ‘Grand Nain’ (AAA, Cavendish subgroup) where</p><p>the soil has dried sufficiently to stop leaf emergence and leaf gas exchange. In roots, in soil</p><p>dry enough to stop leaf emergence, Turner and Thomas (1998) found the osmotic potential</p><p>was -1.0 MPa. The soil had a matric potential of -0.06 MPa. Thus the banana root should be</p><p>able to withdraw water from soil even when leaf gas exchange and leaf emergence have</p><p>ceased because there is a negative gradient in Ψw from the soil to the root. If the roots were</p><p>unable to withdraw water from drying soil, then it would not be possible for the banana plant</p><p>to remain highly hydrated as the soil dries. It is therefore unlikely that the capacity of banana</p><p>roots to withdraw water from dry soil is a reason for the sensitivity of the plant to soil water</p><p>deficit.</p><p>Robinson (1996) points out that bananas have rapid physiological responses to soil water</p><p>deficit and this is the feature that is most likely to determine the response of the crop to</p><p>irrigation. The most sensitive indicator of soil water deficit in banana is the rate of emergence</p><p>of the new leaf (Kallarackal et al., 1990; Hoffmann and Turner, 1993; Turner and Thomas,</p><p>1998). If the soil dries rapidly, the leaf may stop emerging after 2 to 10 d and if it dries</p><p>slowly, leaves may stop emerging after 23 d. In the experiments of Hoffmann and Turner</p><p>(1993) a 21 kPa reduction in soil Ψw halved the rate of leaf emergence but a 40 kPa reduction</p><p>in soil Ψw was needed to halve transpiration rate. Thus the rate of emergence of the new leaf</p><p>is a sensitive indicator of drying soil, more so than the closing of stomata.</p><p>Bananas remain highly hydrated even when the soil is dry and so there needs to be a</p><p>mechanism by which this occurs. Thomas (1995) grew bananas cv. ‘Williams’ (AAA,</p><p>Cavendish subgroup) with a split root system and showed that if half of the roots were</p><p>exposed to drying soil, then the stomata closed, even though the leaves were well hydrated.</p><p>Severing the roots that were exposed to the dry soil opened the stomata, indicating a signal</p><p>from roots to shoots that closed them. By this mechanism the banana would be able to sense</p><p>drying soil and begin to close its stomata. This would reduce water loss from the leaves, but it</p><p>does not explain why the plant remains highly hydrated because the data of Bananuka et al.</p><p>(1999) show that if a leaf is severed from a banana plant then it will lose from 24 to 76% of</p><p>its weight (primarily water) after 48 h of drying, depending on the genotype. This is a high</p><p>rate of water loss considering that in the field the loss of water from intact leaves on banana</p><p>plants (cv. ‘Dwarf Cavendish’, AAA, Cavendish subgroup) was only 10% even though they</p><p>David W. Turner, Jeanie A. Fortescue and Dane S. Thomas</p><p>18</p><p>were subjected to a reduction of 70% in available water in the soil over 10 d (Shmueli, 1953).</p><p>This implies that the root system has an important role to play in keeping the plant hydrated</p><p>even when the soil is drying. The mechanism by which this might occur is that once the</p><p>stomata are closed, root pressure becomes the dominant force supplying water</p>