Vegetative Development, Primary and Secondary Growth of the Shoot System of Young Terminalia Superba Tropical Trees, in a Natural Environment

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Vegetative development, primary and secondary growth of the shoot system of young Terminalia superba tropical trees, in a natural environment. I. Spatial variation in structure and size of axes E de Faÿ

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E de Faÿ. Vegetative development, primary and secondary growth of the shoot system of young Terminalia superba tropical trees, in a natural environment. I. Spatial variation in structure and size of axes. Annales des sciences forestières, INRA/EDP Sciences, 1992, 49 (4), pp.389-402. hal-00882811

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Vegetative development, primary and secondary growth of the shoot system of young Terminalia superba tropical trees, in a natural environment. I. Spatial variation in structure and size of axes

E de Faÿ

Université de Nancy I, Laboratoire de biologie des Ligneux, BP 239, 54506 Vandœuvre-lès-Nancy Cedex, France

(Received 21 August 1991; accepted 17 April 1992)

Summary — Spatial variations in trunk structure including wood histology and size of axes were examined in 5 21-month-old Terminalia superba Engl and Diels trees, grown in a natural tropical environment. Long and shorter internode series alternated along the main axes, forming rather poorly delimited units of extension. In trunk wood, the paratracheal axial parenchyma of the confluent type formed irregular bands, the spacing of which varied gradually, increasing and decreasing alternately. These widely- and narrowly- spaced parenchyma bands differentiated various wood layers. The radial enlargement and wall thickness of fibres also varied in the same manner, as did, but to a lesser extent, the width of parenchymal bands, the radial enlargement of parenchyma cells and vessels, and the wall thickness of vessels. The number of various wood layers in trunk segments that were defined by variations in intemodal length was not related to the order of appearance of the trunk segments in question. These results suggest that trunk wood exhibited alternating dense and not very dense wood layers, but they did not provide visible structural evidence of a well-pronounced growth periodicity in the main shoot of Terminalia superba. The existence of a structural discontinuity in the peripheral wood and the significance of the basipetal differentiation of the outermost adjacent wood layer have been discussed in relation to seasonal changes in climate and phenology. On the other hand, trunk thickness increased markedly from 5 cm above to 5 cm beneath the upper pseudo- whorls of branches. The thickness of axes (branches and trunks) was closely related to the number of sympodial units located in a centrifugal and an upper position respectively. Moreover, a pseudo- whorl of branches was generally inserted in the middle part of trunk segments defined by variations in internodal length. These data indicate trunk-branch correlations. It is suggested that some structural variations in trunk wood could be related to branching. radial size / structural unit / Terminalia superba / tropical tree / wood

Résumé — Développement végétatif, croissance primaire et secondaire du système cauli- naire de jeunes arbres tropicaux de l’espèce Terminalia superba, dans un environnement naturel. I. Variation dans l’espace de la structure et de la dimension des axes. Les variations dans l’espace de la structure du tronc - y compris l’histologie du bois - et de la dimension des axes furent examinées chez 5 plants de Terminalia superba Engl et Diels âgés de 21 mois et poussant dans un environnement naturel tropical. Des séries d’entre-nœuds longs et plus courts alternaient le long des axes principaux formant des unités de croissance mal délimitées. Dans le bois des troncs, le parenchyme axial paratrachéal, de type confluent, formait des bandes irrégulières dont l’espacement variait graduellement, augmentant et diminuant en alternance. Ces bandes de parenchyme largement et fai- blement espacées différenciaient des couches de bois. La dilatation radiale et l’épaisseur des parois des fibres variaient aussi de la même manière que précédemment. Il en était de même, quoique à un moindre degré, de l’épaisseur des bandes de parenchyme, de la dilatation radiale des cellules paren- chymateuses et des vaisseaux, et de l’épaisseur des parois des vaisseaux. Le nombre de couches de bois dans les segments de tronc définis par des variations dans la longueur des entre-nœuds n’était pas lié à l’ordre d’apparition des segments en question. Tous ces résultats suggèrent que le bois des troncs présentait des couches alternativement denses et peu denses, mais ils ne donnent pas de preuve structurale d’une périodicité de croissance bien marquée dans la flèche des Terminalia superba. L’existence d’une discontinuité structurale dans le bois périphérique et la signification de la couche de bois adjacente la plus externe sont discutées en relation avec les changements de saison et de phénologie. Par ailleurs, l’épaisseur des troncs s’accroissait de façon marquée de 5 cm au- dessus à 5 cm en-dessous des étages supérieurs de branches. L’épaisseur des axes (branches et troncs) était étroitement liée au nombre d’unités sympodiales en position respectivement centrifuge et supérieure. De plus, un étage de branches était généralement inséré dans la partie médiane des segments de tronc définis par des variations dans la longueur des entre-nœuds. Ces données attirent l’attention sur les corrélations entre branches et tronc. II est suggéré que des variations structurales dans le bois du tronc pourraient être liées à la ramification. dimension radiale / unité structurale /Terminalia superba / arbre tropical / bois

INTRODUCTION cambial growth among the trees of the intertropical zone. However, detailed studies on Some attention has been paid to growth cambial activity, such as histophysiological phenomena in tropical trees. Morphological investigations are still rare, fragmentary and concern mature trees in- and morphogenetic studies on shoot growth generally growing have demonstrated the basic knowledge of termittently, the wood of which displays annual Paliwal and continuous and flushing - or rhythmic - growth rings (Lowe, 1968; growth and architectural models (Bond, Prasad, 1970; Lawton and Lawton, 1971; 1942; 1945; Scarrone, 1965; Hallé and Rao, 1972; Amobi, 1973; Paliwal et al, Martin, 1968; Borchert, 1969; Hallé and 1976; Ghouse and Shamima Hashmi, 1979; Oldeman, 1970; Greathouse et al, 1971; Zamski, 1979; Rao and Dave, 1981; Rog- Vogel, 1975a,b; Hallé et al, 1978; Ng, 1979; ers, 1981; Dave and Rao, 1982; Desh- Parisot, 1988; El-Morsy and Millet, 1989). pande and Rajendrababu, 1985; Venugopal Concerning secondary growth, there is and Krishnamurthy, 1987). As regards correlations between re- some information on wood production and growing organs, only between leaf and shoot on the existence, anatomy and periodicity lationships growth have been examined in a few trees of growth rings in the wood of numerous tropical species (Hummel, 1946; Mariaux, 1967; (Greathouse et al, 1971; Prévost, 1972; Lowe, 1968; Mariaux, 1969, 1970; Gill, Borchert, 1973, 1978) and the effect of 1971; Amobi, 1974; Détienne et Mariaux, leaves on internode elongation has been 1975, 1976, 1977; Fahn et al, 1981; Mari- demonstrated in Terminalia superba (Mail- lard aux, 1981; Zamski, 1981; Ash, 1983a, b; de et al, 1987b). Faÿ, 1985; Boninsegna et al, 1989; Dé- Young plants of the African species Ter- tienne, 1989; Jacoby, 1989; Worbes, 1989). minalia superba Engl and Diels grown in a These data suggest various patterns of natural environment were studied within the context of research on growth rhythms MATERIALS AND METHODS and relationships between primary and of the shoot T secondary growths system. The trees studied came from the experimental superba is a forest species, the architec- plantation of the Centre Technique Forestier ture of which has been characterized by Tropical on the Ivory Coast, located in the forest Hallé and Oldeman (1970) as Aubréville’s of Anguédédou, about 30 km north-west of Abid- model. Its trunk is a monopode, the growth jan. A clonal plot was put at the author’s dispo- of which is assumed to be rhythmic and sal to study 5 trees. The trees were descended from stem cuttings that had been made from 3- branches a gives pseudowhorled arrange- month-old shoots and had been planted 3 called a tier. Branches ment, commonly months later. They were aged 21 months when are sympodial and horizontal by apposition studied. A good size, well-separated tiers of to spiral phyllotaxy units. Each sympodial branches and an absence of any trunk reitera- unit is characteristic of the genus Terminal- tion were the criteria for the choice of plants. ia, the Terminalia branching being specifi- The clonal origin was unknown at the time of se- lection, which should have ensured a certain cally described in T catappa (Hallé and variability among the chosen trees, as if seed- Oldeman, 1970; Tomlinson and Gill, 1973; lings had been studied. The 5 trees (TA-TE) Fisher, 1978). The vegetative development were of the same geographic provenance, 2 of T superba, at an early stage, has recent- were half-sibs (TA and TC) and 2 were of the ly been studied under controlled conditions same clone (TD and TE). The ground had been (Maillard, 1987; Maillard et al, 1987a,b; prepared, before planting, by manual cutting of the forest the was 2.5 1989). These authors determined the most plot; plant spacing initially x 2.5 m; manual weeding had been regular. favourable conditions for and con- growth Therefore, the T superba trees were not growing sidered growth periodicity. It appears that in competition for light with other vegetation. the trunk displays an alternation of long They had been subjected to full sunlight. and short internode series, obvious at As the species T superba is disseminated 27 °C and under 14- or 16-h daylengths. throughout the evergreen rain forest in the south of the Ivory Coast and it invades the secondary This paper reports a study on the spatial bush (Aubréville, 1959), the variability and local aspects of growth in a natural tropical envi- growing conditions of the trees studied were ap- ronment. The purpose was not only to com- parently similar to those of ’fraké’ saplings - fra- pare the vegetative development of young ké is the local common name of this species - in a chablis of the forest. The site is trees under natural and controlled environ- large adjacent located in the zone at about 5° lati- mental the formation intertropical conditions, especially tude north, that is to say in the so-called ’humid of discrete incre- morphologically growth tropics’. As in many tropical regions, the season- ments (units of extension, Hallé et al, 1978), al variations in temperature and solar radiation but also to increase the number of criteria are not great, but the amount of rainfall is distrib- which would allow the growth of Terminalia uted irregularly. There are 2 dry seasons (De- superba to be characterized. Trunk wood cember-March and mid July-September) alter- with 2 seasons (April-mid July and structure and size of axes were thus investi- nating rainy mid September-November). Thus for more than On the one be- gated. hand, relationships one and a half years, the young trees had been tween radial size of axes and number of subjected to a monthly temperature of 25-28 °C branch modular components, ie sympodial (Atlas de la Côte d’Ivoire, 1978) and a photoperi- units, were sought in addition to units of ex- od of 12.2-13.2 h daylength, allowing for dawn tension along trunks. On the other hand, and dusk (Longman and Jenik, 1963), which is close to the 27 °C and 14-h on trunk wood fairly daylength histological investigations found to be the most favourable for the develop- were aimed at structural variations in finding ment of young T superba trees under controlled relation to units of extension, ie rhythmic conditions (Maillard et al, 1987a). However, they growth rings (de Faÿ, 1985). had lived through several dry seasons and the last one was just before the examination. The served along the trunks, except at the top; lack of rainfall could thus have restricted plant indeed, there was only a sharp limit at the growth seasonally. base of the developing part, in 4 out of 5 For observations and measurements, trunks trees. However, on the lower part, there were cut at the base, at the of March, beginning were several areas with some relatively after total new of the and just leafing plants, short internodes, compared with the were inspected immediately from base to apex. adjacent Variations in internodal The relative position of leaf-scars, or leaves in regions. the upper part only, was studied to find regions length occurred progressively. It should be with short internodes or an alternation of long noted that a slight variation might pass un- and shorter internode regions. The transition noticed and, moreover, leaf-scars tended zones from to short internode were long regions to become indistinct on the old parts of marked to delimit units of extension. When the trunks. Nevertheless, trunk segments con- limit was not obvious, the middle of the shortest of internode series internode was taken into account to separate sisting long separated successive trunk segments, and these were by shorter internode series could be distin- measured. In addition, the number of tiers per guished (fig 1). unit, the number of branches per tier, the num- These delimited gener- ber of sympodial units per branch, the mean ba- poorly segments sal diameter of branches and the circumference ally bore one tier of branches located in of trunks at 5 cm above and below each tier, or the central part. However, 2 sets of in the middle of a unit with no branch, were re- branches were observed in 2 different seg- corded. ments and, in the basal segments, some- For histological studies of the wood, 2 kinds times no branch was found (fig 1). of were collected in the middle of sample part axis the circumfer- each unit of extension, beneath the tier of Concerning sizes, ence of trunks increased from to branches: discs and cores. Firstly, the 2-3-cm apex long discs were put into an air-conditioned room base but irregularly on each side of the de- to dry; afterwards, they were treated with sodi- veloping tiers of branches. In addition, the um hypochlorite to lighten them (Mariaux, 1969) basal diameter of branches was correlated and finely polished; they were observed with a positively with the number of component before and after treatment stereomicroscope units A close with phloroglucinol-HCl, characterizing lignins sympodial (fig 2). relationship was trunk (Sass, 1958). Secondly, the outermost trunk tis- also found between circumfer- sues, including wood, were sampled with a ence and the total number of sympodial bone puncture surgical instrument and the units in the branches inserted above the cores were fixed in Craf 1 (Sass, 1958); they level studied (fig 3). were then cut transversely with a freezing mi- crotome, and the 40-μm thick sections were stained with phloroglucinol-HCl and examined microscopically. Structural variations in trunk wood

The wood of the trunks showed con- RESULTS slight centric colour variations in polished transverse sections. A stereomicroscope high- numerous concentric Spatial variations lighted light irregular bands on a dark back- in external structure and size of axes comparatively ground (figs 4A, B). These bands were paratracheal axial parenchyma of the con- Typical units of extension, ie trunk seg- fluent type. In general, band spacing var- ments, well-delimited by areas of more ied gradually, increasing and decreasing tightly packed leaf-scars, could not be ob- alternately. The dark background of the

polished transverse sections of wood con- sisted of wood fibres. Positive phloroglucinol-HCl tests showed wood fibres ar- ranged in alternating concentric layers (fig 5A). These variations resulted mainly from changes in the number of cells per unit area (fig 5B). These 2 types of concentric and repeat- ed variations - in the spacing of parenchyma bands and in the intensity of staining - were not always closely correlated, especially in the lower trunk segments. More- over, the thickness of wood layers varied strongly within a trunk section, particularly in the lower segments: a single wood layer was sometimes thick and sometimes thin; the different wood layers that were defined by the same feature had very different thicknesses, in the internal wood, whatever their position; the thickness of adjacent wood layers varied independently: for in- stance the wood layers with relatively narrow band spacing were sometimes thick and sometimes thin in comparison with the innermost ones with wider band spacing. The great structural variability in trunk wood made the wood layer count difficult. Several counts of the wood layers that were defined by variations in band spacing were made in each trunk sections (on the 2 polished areas), because a small local variation of band spacing could at first pass unnoticed. The results (table I) showed clearly that the number of wood layers increased basipetally but irregularly from one trunk segment to the next (older one) below. The most recent wood layers (2-5 ac- cording to the trunk level) were distin- guished from each other more easily: those with a wide spacing of parenchyma bands were thick, whereas those with narrow band spacing were thin; moreover, parenchyma bands were wider in the former than in the latter (figs 4A, B). The staining of the wood background following

the phloroglucinol-HCl test was less in- walled fibres, the former belonging to the tense in the wood layers with wide band outermost wood layer that was defined by spacing than in those with narrow band narrowly-spaced parenchyma bands and spacing. Variations in staining were gradu- the latter to the differentiating wood which al from one wood layer to another, except exhibited widely-spaced parenchyma bands between the 2 most recent wood layers (fig 6B). This boundary was not always uni- (fig 6A). form at the cellular level, mainly because Indeed, the limit was sharp only be- of the occurrence of parenchyma bands. In tween the 2 most recent wood layers. His- this area, parenchyma cells changed from tologically, this was the transition between a radially flattened type to a radially dilated strongly radially flattened, thick-walled fi- type - more precisely from a rather narrow bres and younger radially dilated, thinner- area to a wider area in cross section (fig 6B) - and vessels from small, thick-walled by alternating series of long and shorter in- pores to large, relatively thin-walled pores ternodes, as in a controlled environment (fig 6A). The microscopical examination chamber (Maillard et al, 1987a), which did not indicate noticeable changes in wall generally formed poorly-delimited units of staining. Histological differences between extension. The vaguely segmented struc- wood layers with narrow and wide spac- ture of the trunk was confirmed at the ings of parenchyma bands tended to be wood level. The spacing of parenchyma less visible in internal wood (figs 4A, B, 5A, bands, the radial enlargment of wood fi- B). The developing wood layer was found bres and parenchyma cells, the wall thick- in the 5 trunks studied, but its thickness ness of wood fibres and to a lesser extent decreased basipetally and it could be par- the width of parenchyma bands, the pore tially formed or totally missing in the base size and wall thickness of vessels changed of the trunk (figs 4A, B). in such a way that wood layers were suggested to be alternately more and less dense. The changes were generally gradu- DISCUSSION al and apparently bore no relation to the development of the units of extension. The trunk of young T superba trees grown Thus, there were no rhythmic growth rings in a natural environment was characterized in the juvenile wood of T superba, unlike that of Hevea brasiliensis (de Faÿ, 1985; rings of some mature tropical trees (Mari- 1986). In short, structural units of the He- aux, 1967; Boninsegna et al, 1989; Dé- vea type, characteristic of the rhythmic tienne, 1989; Vetter and Botosso, 1989; growth-habit were found neither externally Worbes, 1989). In fact, the abrupt (spatial) along the trunk nor in trunk wood. variations of trunk thickness were related Nevertheless, the structural variations to the upper tiers of branches and there in wood could indicate that the cambial was a close relationship between trunk growth of trunks was alternately rapid and thickness and size of branches (in number slow, especially since structural variations of modules) that were inserted above the of that nature are visible within the growth level studied. Moreover, trunk segments that were defined by variations in inter- al, 1971; Vogel, 1975a, b; de Faÿ, unpub- nodal length usually bore 1 tier of branch- lished results) or Quercus robur (Payan, es. These data indicate trunk-branch cor- 1982; Champagnat et al, 1986). These re- relations and imply that some structural sults on spatial variations in structure and variations in trunk wood could be related to size of axes indicate trunk-branch correla- branching. Indeed, the leaves of develop- tions rather than typical units of extension ing axes are assumed to produce the stim- along the trunk and rhythmic growth rings in uli (phytohormones) that induce the differ- trunk wood. A subsequent study of temporal entiation of wood (Aloni, 1989). aspects of growth in young T superba trees Climatic variations could also have had in the same natural environment (de Faÿ, has results in accor- repercussions on wood formation, espe- 1992) already given dance with the data. It is thus cially the lack of rainfall, as in the wood of present sug- Carya glabra where the spacing of tangen- gested that the ’pagoda’ architecture of Ter- tial parenchyma bands is related to the minalia superba resulted more from the of than from a rate of rainfall (Hill, 1982). At any rate, the periodicity branching flushing outer structural discontinuity in the trunk growth of trunk, at least in the early stage. wood of the trees studied could be related to a seasonal change, at least in phenolo- ACKNOWLEDGMENTS gy. Indeed, initiation of the basipetally developing wood layer was associated in time with the bud break (this had begun 2 The author is grateful to the late Director of the weeks before sampling and had followed Centre Technique Forestier Tropical on the Ivo- the totally leafless period occurring at the ry Coast, Dr K Diabate and his colleagues for JM Favre end of the Reduction or providing plant material and Professor long dry season). of for his critical of absence of the wood at (University Nancy I) reading developing layer the manuscript. the base of trunks should indicate a delay in the resumption of cambial activity, because of the decrease in leaf hor- basipetal REFERENCES mone stimulation (Aloni, 1989). 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