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Anatomy and Morphology |
2 IRD, UMR AMAP (botAnique et bioinforMatique de l'Architecture des Plantes), Montpellier F-34000 France 3 Departamento de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia 4 École Nationale du Génie Rural des Eaux et des Forêts, 648, rue Jean-François Breton, BP 7353-34086 Montpellier Cedex 4, France 5 INRA, UMR AMAP, Montpellier F-34000 France
Received for publication 17 August 2007. Accepted for publication 15 January 2008.
ABSTRACT
Cecropia species, ranging from Mexico to northern Argentina and the West Indies, are pioneer trees that colonize cleared areas with high light. To determine their ages to help pinpoint the date of the area's disturbance, we need to understand their developmental and architectural changes over time. The simple architecture of Cecropia conforms to the model of Rauh; that is, it has orthotropic axes with lateral flowering and rhythmic branching. The axes are made of a succession of nodes and internodes whose length and associated lateral productions remain measurable for years. Thus, by describing the tree trunk node by node, we can depict the sequence of events involved in tree development. For 25 trees of C. sciadophylla, from two stations in French Guiana and Colombia, we recorded internode length and any presence of branches, and flowers for each node. Using autocorrelation coefficients, we found a high periodicity in flowering and branching, with inflorescences at every 25 nodes, stages of branches spaced by a multiple of 25 nodes, and alternation of long and short nodes every 25 nodes. Considering that flowering is annual for many Cecropia species, the main conclusion of this work is that C. sciadophylla has strong annual growth, branching, and flowering rhythms. In addition, the age of the tree can be estimated retrospectively by observing its adult morphology.
Key Words: Colombia • French Guiana • gap age • periodicity • phenological processes • plant morphology • synchronicity • Urticaceae
Plant phenology can be defined as the study of the timing of recurring biological events, its causes with regards to biotic and abiotic forces, and the relation among phases of the same or different species (Leith, 1974
). Classic studies on phenology are centered on the observation of processes such as flowering/fructification or foliation/defoliation in deciduous species (Wallace and Painter, 2002; Bawa et al., 2003; Hamann, 2004). Other events with a temporal pattern, such as growth expression (in terms of timing of elongation and variability in length or number of nodes elongated), ramification, nectar secretions, and germination are also part of this field of investigation (Sabatier and Puig, 1986; Loubry, 1994).
Methods employed in phenological studies usually consist of (1) compilation of herbarium data (Croat, 1975; Borchert, 1996; Primack et al., 2004), usually including rather imprecise information (e.g., ripe and unripe stages are rarely differentiated) and (2) observations over local plant populations, which occasionally include monitoring growth over long periods (Croat, 1975; Van Schaik et al., 1993; Newstrom et al., 1994; Sakai, 2001). However, an alternative approach not much documented for tropical species is a posteriori reconstruction of individual development by observation of morphological or macroanatomical markers that can be interpolated as the functional history of meristems (Hallé et al., 1978; Barthélémy and Caraglio, 2007). For instance, in the case of rhythmical growth (i.e., alternation between elongation and rest phases), growth suppression is often observed on axes as small internodes, modified leaves, cataphyll scars in rings (i.e., modified leaves that protect apical bud during rest phases), or changes in pith color on a longitudinal section of the stem. Using these markers, we can delimit growth units and measure their characteristics (e.g., length and number of nodes). Additionally, processes of ramification or flowering also leave characteristic scars, which vary in appearance with time and species.
In temperate zones, growth is usually rhythmical, synchronous, and periodic due to seasonal constraints (Hallé et al., 1978; Richards, 1996; Sakai, 2001). Scars left by buds during winter, can be used to delimit years and to reconstruct retrospectively plant development during long periods (Heuret et al., 2000, Heuret et al., 2006; Nicolini et al., 2001; Sakai, 2001, Passo et al., 2002). In this way, plant topology can be better understood within a temporary frame. The implications of this approach are numerous because it may allow estimates of tree age and provide advance knowledge about growth, ramification, and flowering processes during plant ontogeny. In spite of the fact that topological approaches can complement, and even replace, monitoring growth studies, such approaches have not been widely used. In tropical zones, the diversities in plant development are expressed more continuously in time than in temperate latitudes. Thus, we can observe great variability in the expression of growth, ramification, and flowering processes (Comte, 1993; Edelin, 1993; Van Schaik et al., 1993; Loubry, 1994; Sakai, 2001). When growth is rhythmic, alternation between elongation and resting phases can be either periodic or irregular. At the individual level, axes can grow either synchronously or each one at its own rate. Thus, in tropical rain forests, plant topology at a fine level can be described according to available morphological markers, but it is difficult to ensure a temporary connotation from retrospective observations (Hallé et al., 1978). However, a precise analysis of plant structure using statistical models may allow one to reveal information that is hidden in empirical data (because of noise and combinatorial complexity related to multivariate observation). These hidden regularities enable researchers to make strong assumptions on the rules of plant construction in time (Guédon et al., 2001; Heuret et al., 2002).
The neotropical genus Cecropia Loefl., includes 61 species, distributed from southern Mexico to northern Argentina, with some species occurring in the Antilles (Wheeler, 1942; Berg, 1978; Berg, 2000; Berg and Franco, 2005; Stevens, 2007). It is the most important genus of pioneer trees in the neotropics; it grows rapidly and ably colonizes gaps (Álvarez-Buylla and Martínez-Ramos, 1992; Whitmore, 1998). Cecropia trees are dioecious plants, usually with a candelabrum-like branching system, following the architectural model of Rauh (Hallé and Oldeman, 1970; Hallé et al., 1978). Branching axes are orthotropic, with lateral flowering and rhythmic branching. Recent studies have shown that C. obtusa is highly regular in growth, ramification, and flowering (Heuret et al., 2002). From a retrospective reconstruction of its developmental pattern and the use of statistical tools borrowed from time series analyses (Guédon et al., 2001, 2003), Heuret et al. (2002) showed that the rate of node production, flowering, and ramification are respectively synchronous for sets of axes within an individual of C. obtusa. Additionally, they suggested that flowering and ramification processes are annual and synchronous at the population level. In this work, we focused on a second species of this genus, C. sciadophylla, characterized by a high life expectancy compared to other species of Cecropia and by a widespread distribution throughout the Amazonian basin, the Llanos region of Colombia and Venezuela, and the Guiana region (i.e., from French Guiana to eastern Venezuela). The objectives of this study were (1) to determine and compare the patterns of growth, ramification, and flowering for C. sciadophylla individuals in two populations, (2) to determine if the model of growth of C. sciadophylla is similar and comparable to the model of growth of C. obtusa, and (3) to propose a phenological hypothesis of development in Cecropia based on its architecture.
MATERIALS AND METHODS
Study site
Two populations of Cecropia sciadophylla, one in French Guiana and a second in Colombia, were studied. The French Guiana population was located at Saint-Elie road (5°30' N, 53° W), at ~16 km from Sinnamary. Climate in French Guiana is seasonal with a 3-mo dry season from mid-August to mid-November and a rainy season during the other 9 mo. Additionally, a short dry season may occur in February and March (Boyé et al., 1979). Mean annual rainfall is 3000 mm/yr. The Colombian population was located at Tinigua National Park on the east margin of the Guayabero River (La Macarena, department of Meta, 2°40' N, 74°10' W). Rainfall regime at Tinigua National Park is seasonal with a 2–3-mo dry period between December and March and a mean rainfall of 2782 mm/yr (Stevenson, 2006) (Fig. 1).
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). Individual trees can reach 30 m in height, phyllotaxy is alternate with a 5/12 spiral phylotactic fraction. The leaves are stipulate, large, and peltate. There are three lateral buds in the axil of each leaf (Fig. 2). The central bud is vegetative and may potentially give rise to a branch. Buds on each side correspond to two prophyllar axillary buds and may give rise to inflorescences, which are thus arranged in pairs, each comprising a set of spikes. Pistillate inflorescences have 3–6(10) spikes and staminate inflorescences have 8–15 spikes (Berg and Franco, 2005).
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Plant material and measurements
Nineteen individuals (six pistillate and thirteen staminate) were felled and measured at Saint-Elie, while six individuals (four pistillate and two staminate) were measured at Tinigua Park. Only straight trees without any evident trauma were selected and felled. All data were collected during one week in September 2005 at Saint-Elie (eight observers), and during one week in January 2006 at Tinigua Park (two observers). All staminate and pistillate individuals measured had two or more tiers of branches on the main axis. For all trees, trunk girth at a height of 1.30 m (GBH) was measured, and diameter was estimated assuming a circular cross section (DBH). Tree height and the height and number of nodes until the first tier of branches (present or pruned) and appearance of the first inflorescence were recorded on the fallen tree.
Following Heuret et al. (2002) protocol, trunks formed by a succession of metamers were described node by node from base to top. Because of the frequent development of stilt roots, the number of nodes separating the cotyledons of the first node measured is uncertain. Three variables were recorded for each node: (1) length of the underlying internode, (2) state of the central bud as "0" for no branch and "1" for developed branch (pruned and dead branches were included in this category), and (3) state of the lateral buds as "0" for no inflorescence and "1" for developed inflorescence (detected as either presence of the inflorescence or its scar). Aborted inflorescences and branches were not recorded because criteria to determine these states are rather ambiguous.
Cecropia sciadophylla fructification pattern at Tinigua National Park
Phenological data were collected during three yearly cycles at Tinigua National Park (April 1990–March 1991, August 1996–July 1997, and February 2000–January 2001). The information was recorded in 12 transects (about 450 m each) in which we biweekly observed all C. sciadophylla individuals that had flowers and/or fruits (Stevenson et al., 1998). This information was complemented by feeding observations in C. sciadophylla fruiting trees during the same periods (Stevenson, 2006).
Statistical analysis
Tree topology, i.e., the relative positions of the different botanical units described (nodes and axes), was coded as sequences and analyzed using the AMAPmod software (Godin et al., 1997a, Godin et al., 1997b; Godin et al., 1999).
An interesting statistical tool to separate and characterize growth components is based on the assumption of a decomposition model, in which the ontogenetic growth component and environmental component are combined in an additive manner (Guédon et al., 2007). To analyze fluctuation of internode's length, we used classical methods of time series analysis relying on a decomposition principle. The different sources of variation, such as long-term changes in mean level and local fluctuations, are differentiated by the application of different types of filters that were initially analyzed for individual trees (Chatfield, 2003; for more information about the use of methods to analyze botanical sequences, see Guédon et al., 2007). The common procedure to deal with a trend is to apply a linear filter that converts the measured sequences {xt} into another {yt} by a linear operation
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r ar = 1. This linear operation is often referred to as a moving average, in which a smoothed curve is adjusted. To choose an appropriate filter is difficult and the choice remains partly arbitrary, so it is recommended to try a variety of filters to get a good idea of the underlying trend (Guédon et al., 2007). We chose to use the symmetric smoothing filter corresponding to the probability mass function of binomial distributions with parameters n = 50 and p = 0.5 or n = 100and p = 0.5 to extract the trend of internode length sequences. Having extracted the trend, we looked at local fluctuation by examining the residuals. Residuals were extracted by division instead of substraction as is often done (Fritts, 1976):
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The underlying implicit hypothesis is that fluctuation amplitudes given by |xt – Smooth (xt)| are roughly proportional to the corresponding trend level. This standardization allowed us to give the same status to fluctuations of both small and large amplitudes, which is important in old trees that have very short internodes compared to the first node at the trunk base.
An important tool for exploring sequences built from quantitative variables is provided by a series of quantities called sample autocorrelation coefficients, which measure the correlation between observations separated by different distances. The autocorrelation function measures the correlation between Xt and Xt+k as a function of the lag k. The sample autocorrelation function is an even function of the lag and hence needs to be plotted for k = 0, 1, 2, ... We applied autocorrelation analysis to binary branching and flowering sequences as well as residual sequences obtained from filtered internode length sequences.
Mann–Whitney–Wilcoxon (MWW) nonparametric tests were used to compare tree height, diameter, first branch, and first inflorescence positions between the two populations because it allows comparisons of distributions derived from relatively small samples (Saporta, 1990).
RESULTS
Height, diameter, first branch, and inflorescence positions
Sampled trees had similar heights (mean 22.4 m) and total number of nodes (mean 467.3) in both populations, while stem diameter was significantly higher for trees at Tinigua than at Saint-Elie (Table 1). There were no significant differences in height until the first branch (mean 12.9 m) or the first inflorescence scars (mean 16.4 m) between populations. However, the number of nodes before the first branch or the first inflorescence was significantly higher for Saint-Elie trees than for Tinigua trees. For both populations, the first inflorescences were mainly positioned between the first and the third tier of branches.
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For the internodal lengths, the autocorrelation function calculated on the residues had positive significant maxima at lags of 26, 53, and 107 when the sequences were filtered with a binomial distribution with parameters 50 and 0.5 or 200 and 0.5. The use of a binomial distribution with parameters 50 and 0.5, however, highlighted positive significant maxima at lags of 68, 96, and 124. For a lag ranging from 0 to 75, this function had a strong periodicity of 25 nodes associated with a weaker periodicity of 14 nodes (Fig. 5C).
Fructification pattern of Cecropia sciadophylla at Tinigua National Park
The phenological data collected during three years for 10 individuals at Tinigua Park showed that the flowering pattern of C. sciadophylla is annual (Fig. 6). The peak of reproductive structure production is located in the months of January and February, the driest months for the study area (Stevenson et al., 1998).
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The number of cycles estimated for the studied individuals ranged from 16 to 20 yr for both populations (mean 19 ± 1) (Table 1). However, a remarkable individual of 33 cycles was observed at Saint-Elie. The first tier of branches and the first inflorescence were developed on average after a slightly higher number of cycles in the Saint-Elie population than in the Tinigua population.
Considering the average length of successive cycles (Fig. 7A) and the average cumulative height per cycles (Fig. 7B), there was no significant difference between the two populations. Successive cycle lengths, initially with an average length of 2 m, progressively decreased to reach a stable cycle length of 0.25 m after nearly 20 cycles. At this stage, the height of the tree is around 21 m.
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Our results show a strongly rhythmic and a clear topological periodicity in the spacing of branch tiers, flowers, and internodal elongation, with a period of 25 nodes for trees at Saint-Elie and 23 nodes for trees at Tinigua.
Many studies have suggested a high annual periodicity in flowering and fruit production processes in the genus Cecropia. In Barro Colorado Island (Panama), Milton (1991) described an annual flowering pattern for C. insignis, as did Frankie et al. (1974) and Fleming and Williams (1990), who showed the same pattern for C. peltata in Costa Rica and Cortés (2005) for C. membranacea at Tinigua National Park in Colombia. In all these cases, the flowering/fruit production period extends throughout the dry season. Although we do not know the rate of node production in C. sciadophylla, our results on flowering and fruiting period reinforce these precedent works and allow us to conclude that for the Tinigua population a cycle of 23 nodes in the flowering pattern corresponds to an annual rhythm. The frequency of nodes with developed inflorescence scars according to the node rank from the tip to the base (Fig. 3) also indicate that flowering is synchronous at the population level and that the phyllochron is stable among different trees as well as for individual trees during their ontogeny. By extension, branching pattern and fluctuation in internode lengths, which have the same periodicity of the flowering pattern, correspond to an annual rhythm. These conclusions are very close to the ones issued by Heuret et al. (2002), who found that the flowering and branching processes in C. obtusa are characterized by annual cycles of 35 nodes in French Guiana, based also on a retrospective analysis. In addition, their result was supported by previous work that showed that C. obtusa takes an average of 10 d to produce a new node (Lauri, 1988; Belin-Depoux et al., 1997).
Several elements distinguish the two populations of C. sciadophylla studied. (1) If the two populations seem to have an identical height, the first flowering and branching began earlier (in terms of number of nodes and age) for the Tinigua trees. It is possible that different growth situations, such as the density of individuals in the population, can be the origin of such a difference; many studies have shown that environmental conditions may advance or delay the flowering processes (Barthélémy, 1988; Barthélémy et al., 1995, 1997; Levy and Dean, 1998; Grosfeld et al., 1999; Simpson et al., 1999; Sakai, 2001; Nicolini et al., 2003). (2) Another difference between these populations is the greater diameter for trees of similar ages and sizes at the Tinigua population. This disparity can be caused by different factors. For example, trees from Tinigua Park ramified earlier and bore slightly more branches than do the trees from Saint-Elie. We suspect that because this species is globally poorly branched, minor differences in the number of branches can have a strong repercussion in terms of leaf area over time and can induce strong differences in trunk diameter, which is an integrative variable (Shinozaki et al., 1964; Zimmermann, 1983). Another important factor that can be generating a greater diameter is the soil fertility. Fertile soils tend to become more common toward the Andes, and strong evidence for a positive relation between wood productivity and soil fertility has been found (Malhi et al., 2004). In addition to the period of 25 nodes, the trees of Saint-Elie seem to have another period of 12 nodes. This period was observed on the internode lengths and occasionally in the flowering sequences. For the trees of Tinigua, only one period of 23 nodes was observed.
Annual regularity in both populations has to be questioned based on the environmental factors that influence this periodicity (Borchert et al., 2005). For C. peltata and C. obtusifolia in Costa Rica, Davis (1970) described internode length variations that depended on the amount of annual rain, revealing that the internodes established in the dry season are shorter than those established in the rainy season. In the tropics, the movement of the intertropical convergence zone (ITCZ) produces a periodic change in rainfall that often plays a role as proximate and ultimate cause for tropical plant phenology (Van Schaik et al., 1993). In most tropical regions, a correlation between rainfall regime and plant phenology has been reported (Augspurger, 1981, Augspurger, 1983; Borchert, 1983; Reich and Borchert, 1984; Newstrom et al., 1994; Mduma et al., 2007), which demonstrates the existence of annual patterns of plant reproduction. The fact that two cycles per year (for the internode length variable) can occur at Saint-Elie population, while trees at Tinigua only have one annual rhythm is remarkable. The presence of two flowering periods per year is a recurrent phenomenon for the majority of the individuals in the Saint-Elie population. This second period does not present an evident synchrony between the studied individuals. Although it is possible to find years with two dry seasons at Tinigua National Park, the second dry season is weaker than the second dry season in French Guiana. Environmental factors, which could be the origin of this developmental periodicity in Cecropia, remain an open question; however, rainfall seems to be well correlated to the periodicity of plant development (Davis, 1970; Sakai, 2001).
From our study, based on a retrospective description of plant development, it is difficult to establish a link between the variations observed in an annual period of 25 nodes and annual fluctuations in climate such as rainfall regimes. Indeed, even though we found an annual cycle equivalent to 25 nodes, we cannot affirm that the phyllochron does not fluctuate during the year. The internode length fluctuation seems to indicate the opposite, however, because it is common to associate this character with elongation speed. Thus, if it is possible to establish a link between topology and developmental dynamics, the level of analysis should be annual and should necessarily involve adequate growth monitoring to determine possible intraannual fluctuations.
In this paper we used a protocol of measures similar to the one used by Heuret et al. (2002). The methodological contribution of Heuret et al. (2002) was the use of the autocorrelation coefficients to find periodicity in branching and flowering sequences. In this paper, we used time series analysis that relied on a decomposition principle to separate the ontogenetic and environmental components in sequences of internodal lengths. Combining that analysis with the autocorrelation analysis allowed us to find a high topological periodicity in growth and to propose a phenological developmental hypothesis in C. sciadophylla based on its architecture.
An important application of this study is the possibility of determining the age of C. sciadophylla individuals. Our data suggest that dividing the total number of nodes on the trunk by 25 or 23 is sufficient to determine the age of an individual. Additionally, given what was found for C. obtusa and C. sciadophylla, similar growth patterns may exist in other species of Cecropia, as observed in C. ficifolia (P.-C. Zalamea, unpublished data). The genus Cecropia is associated with the initial phases of neotropical forest regeneration (Berg, 1978; Vázquez-Yanes, 1980; Martínez-Ramos et al., 1988; Álvarez-Buylla and Martínez-Ramos, 1992; Richards, 1996; Brokaw, 1998; Whitmore, 1998; Berg and Franco, 2005), which makes the genus a good candidate for estimating the time since a forest disturbance. Nevertheless, flowering and ramification processes have been poorly studied in the genus. This study suggests the need for similar explorations in other Cecropia species with a wide distribution range and ecological and geographic variation, to evaluate the suitability of using Cecropia trees as a chronometer for dating the ages of neotropical forest gaps, forestry roads, and mining sites.
FOOTNOTES
1 The authors thank S. Martínez, A. Bernacchi, S. Dirou, S. Gerbaud, and C. Vitel for their assistance in the field, with special thanks to Dr. D. Barthélémy and C. Sarmiento for comments and important discussions on earlier drafts of this manuscript. They also thank Dr. Y. Guédon for enlightening discussions during data analyses. Dr. N. Brokaw, M. Zalamea, I. Zalamea and anonymous reviewers made valuable suggestions to improve the manuscript. This research was partially supported by the ENGREF (Kourou) and the CIEM (Centro de Investigaciones Ecológicas La Macarena), Universidad de los Andes. Part of this work was supported by an IRD (Institut de Recherche pour le Développement, France) doctoral grant to P.-C.Z. 
6 Author for correspondence (e-mail: zalamea{at}cirad.fr); TA40/PS2, Bd. de la Lironde, 34398 Montpellier Cedex 5, France; phone: 33 (0) 4.67.61.55.98; fax: 33 (0) 4.67.61.56.68
LITERATURE CITED
Álvarez-Buylla, E. R., AND M. Martínez-Ramos. 1992. Demography and allometry of Cecropia obtusifolia, a neotropical pioneer tree—An evaluation of the climax–pioneer paradigm for tropical rain forest. Journal of Ecology 80: 275–290.[CrossRef][Web of Science]
Augspurger, C. K. 1981. Reproductive synchrony of a tropical shrub: Experimental studies on effects of pollinator and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62: 775–788.[CrossRef][Web of Science]
Augspurger, C. K. 1983. Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15: 257–269.[CrossRef][Web of Science]
Barthélémy, D. 1988. Architecture et sexualitéchez quelques plantes tropicales: Le concept de floración automatique. Ph.D. thesis, UniversitéSciences et Techniques du Languedoc Montpellier 2, Montpellier, France.
Barthélémy, D., AND Y. Caraglio. 2007. Plant architecture: A dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of Botany 99: 375–407.
Barthélémy, D., Y. Caraglio, AND E. Costes. 1997. Architecture, gradients morphogénétiques et âge physiologique chez les végétaux. In J. Bouchon, P. de Reffye, and D. Barthélémy [eds.], Modélisation et simulation de l'architecture des végétaux, Institut National de la Recherche Agronomique, 11–87. Science Update, Paris, France.
Barthélémy, D., S. A. Sabatier, AND O. Pascal. 1995. Le développement architectural du noyer commun Juglans regia L. (Juglandaceae). Forêt Entreprise 103: 61–68.
Bawa, K. S., H. Kang, AND M. H. Grayum. 2003. Relationships among time, frequency, and duration of flowering in tropical rain forest trees. American Journal of Botany 90: 877–887.
Belin-Depoux, M., P.-J. Solano, C. Lubrano, J.-R. Robin, P. Chouteau, AND M.-C. Touzet. 1997. La fonction myrmécophile de Cecropia obtusa Trecul (Urticaceae) en Guyane française. Acta Botanica Gallica 144: 289–313.[Web of Science]
Berg, C. C. 1978. Espécies de cécropia da Amazonia Brasileira. Acta Amazonica 8: 149–182.
Berg, C. C. 2000. Flora de Venezuela. Fundación Instituto Botánico de Venezuela, Caracas, Venezuela.
Berg, C. C., AND P. Franco. 2005. Flora neotropica monograph 94. Cecropia. Organization for Flora Neotropica. New York Botanical Garden Press, Bronx, New York, USA.
Borchert, R. 1983. Phenology and control of flowering in tropical trees. Biotropica 15: 81–89.[CrossRef][Web of Science]
Borchert, R. 1996. Phenology and flowering periodicity of neotropical dry forest species: Evidence from herbarium collections. Journal of Tropical Ecology 12: 65–80.[CrossRef][Web of Science]
Borchert, R., S. Renner, Z. Calle, D. Navarrete, A. Tye, L. Gautier, R. Spichiger, AND P. Von Hildebrand. 2005. Photoperiodic induction of synchronous flowering near the equator. Nature 433: 627–629.[CrossRef][Medline]
Boyé, M., G. Cabaussel, AND C. Yankoses. 1979. Climatologie. In CNRS (Centre National de la Recherche Scientifique)-ORSTOM (Office de Recherche Scientifique et Technique Outre-Mer) [eds], Atlas de la Guyane. Cayenne, French Guiana.
Brokaw, N. V. L. 1998. Cecropia schreberiana in the Luquillo Mountains of Puerto Rico. Botanical Review 64: 91–120.[CrossRef]
Chatfield, C. 2003. The analysis of time series: An introduction, 6th ed. Chapman and Hall/CRC Press, Boca Raton, Florida, USA.
Comte, L. 1993. Rythmes de croissance et structures spatiales périodiques d'arbres tropicaux. Exemple de cinq espèces de forê.équatoriale. Ph.D. thesis, Universitédes Sciences et Techniques du Languedoc Montpellier 2, Montpellier, France.
Cortés, A. I. 2005. Análisis de los patrones de floración de las especies del Parque Tinigua, Colombia. B.Sc. thesis, Universidad de los Andes, Bogotá, Colombia.
Croat, T. B. 1975. Phenological behavior of habit and habitat classes on Barro Colorado Island (Panama Canal Zone). Biotropica 7: 270–277.[CrossRef]
Davis, R. B. 1970. Seasonal differences in internodal lengths in Cecropia trees: A suggested method for measurement of past growth in height. Turrialba 20: 100–104.[Web of Science]
Edelin, C. 1993. Aspects morphologiques de la croissance rythmique chez les arbres tropicaux. Compte Rendu du Séminaire du groupe d'Etude de l'Arbre: Le rythme de croissance, base de l'organisation temporelle de l'arbre. INRA (Institut National de la Recherche Agronomique), Angers 25–26: 13–23.
Fleming, T. H., AND C. F. Williams. 1990. Phenology, seed dispersal, and recruitment in Cecropia peltata (Moraceae) in Costa Rican tropical dry forest. Journal of Tropical Ecology 6: 163–178.[CrossRef][Web of Science]
Frankie, G. W., H. G. Baker, AND P. A. Opler. 1974. Comparative phenological studies of trees in tropical wet and dry forest in the lowlands of Costa Rica. Journal of Ecology 62: 881–919.[CrossRef][Web of Science]
Fritts, H. C. 1976. Tree rings and climate. Academic Press, London, UK.
Godin, C., E. Costes, AND Y. Caraglio. 1997a. Exploring plant topological structure with the AMAPmod software: An outline. Silva Fennica 31: 355–366.
Godin, C., Y. Guédon, AND E. Costes. 1999. Exploration of plant architecture databases with the AMAPmod software illustrated on an apple tree hybrid family. Agronomie 19: 163–184.[CrossRef][Web of Science]
Godin, C., Y. Guédon, E. Costes, AND Y. Caraglio. 1997b. Measuring and analyzing plants with AMAP-mod software. In M. T. Michalewicz [ed.], Advances in computational life sciences, vol. 1, Plants to ecosystems, 63–94. CSIRO, Melbourne, Australia.
Grosfeld, J., D. Barthélémy, AND C. Brion. 1999. Architectural variations of Araucaria araucana (Molina) K. Koch (Araucariaceae) in its natural habitat. In M. H. Kurmann, and A. R. Hemsley [eds.], The evolution of plant architecture, 109–122. Royal Botanic Gardens, Kew, UK.
Guédon, Y., D. Barthélémy, Y. Caraglio, AND E. Costes. 2001. Pattern analysis in branching and axillary flowering sequences. Journal of Theoretical Biology 212: 481–520.[CrossRef][Web of Science][Medline]
Guédon, Y., Y. Caraglio, P. Heuret, E. Lebarbier, AND C. Meredieu. 2007. Analyzing growth components in trees. Journal of Theoretical Biology 248: 418–447.[CrossRef][Medline]
Guédon, Y., P. Heuret, AND E. Costes. 2003. Comparison methods for branching and axillary flowering sequences. Journal of Theoretical Biology 225: 301–325.[CrossRef][Web of Science][Medline]
Hallé, F., AND R. A. A. Oldeman. 1970. Essai sur l'architecture et la dynamique de croissance des arbres tropicaux. Masson, Paris, France.
Hallé, F., R. A. A. Oldeman, AND P. B. Tomlinson. 1978. Tropical trees and forest. Springer-Verlag, Berlin, Germany.
Hamann, A. 2004. Flowering and fruiting phenology of a Philippine submontane rain forest: Climatic factors as proximate and ultimate causes. Journal of Ecology 92: 24–31.[CrossRef][Web of Science]
Heuret, P., D. Barthélémy, Y. Guédon, X. Coulmier, AND J. Tancre. 2002. Synchronization of growth, branching and flowering processes in South American tropical tree Cecropia obtusa (Urticaceae). American Journal of Botany 89: 1180–1187.
Heuret, P., D. Barthélémy, E. Nicolini, AND C. Atger. 2000. Analyse des composantes de la croissance en hauteur et de la formation du tronc chez le chêne sessile, Quercus petraea (Matt.) Liebl. (Fagaceae) en sylviculture dynamique. Canadian Journal of Botany 78: 361–363.[CrossRef]
Heuret, P., C. Meredieu, T. Coudurier, F. Courdier, AND D. Barthélémy. 2006. Ontogenetic trends in the morphological features of main stem annual shoots of Pinus pinaster (Pinaceae). American Journal of Botany 93: 1577–1587.
Lauri, P.-E. 1988. Le mouvement morphogénétique, approche morphométrique et restitution graphique. L'exemple de quelques plantes tropicales. Ph.D. thesis, UniversitéSciences et Techniques du Languedoc Montpellier 2, Montpellier, France.
Leith, H. 1974. Phenology and seasonality modeling. Springer, Berlin, Germany.
Levy, Y. Y., AND C. Dean. 1998. The transition to flowering. Plant Cell 10: 1973–1989.
Loubry, D. 1994. Déterminisme du comportement phénologique des arbres en fôret tropicale humide de Guyane Française (5°lat. N), Paris. Ph.D. thesis, Universitéde Paris VI, Paris, France.
Malhi, Y., T. Baker, O. Phillips, S. Almeida, E. Alvarez, L. Arroyo, J. Chave, I. Czsimczik, A. Di Fiore, N. Higuchi, T. Killeen, S. Laurance, W. Laurance, S. Lewis, L. Mercado, A. Monteagudo, D. Neill, P. Nuñez, S. Patiño, N. Pitman, C. Quesada, R. Salomão, J. Macedo, A. Torres, R. Vasquez, J. Terborgh, B. Vinceti, AND J. Loyd. 2004. The above-ground coarse wood productivity of 104 neotropical forest plots. Global Change Biology 10: 563–591.[CrossRef][Web of Science]
Martínez-Ramos, M., E. R. Álvarez-Buylla, J. Sarukhan, AND D. Pinero. 1988. Treefall age determination and gap dynamics in tropical forest. Journal of Ecology 76: 700–716.[CrossRef][Web of Science]
Mduma, S., A. Sinclair, AND R. Turkington. 2007. The role of rainfall and predators in determining synchrony in reproduction of savanna trees in Serengeti National Park, Tanzania. Journal of Ecology 95: 184–196.[CrossRef][Web of Science]
Milton, K. 1991. Leaf change and fruit production in six neotropical Moraceae species. Journal of Ecology 79: 1–26.[CrossRef][Web of Science]
Newstrom, L. E., G. W. Frankie, AND H. G. Baker. 1994. A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica 26: 141–159.[CrossRef][Web of Science]
Nicolini, E., Y. Caraglio, R. Pélissier, C. Leroy, AND J. C. Roggy. 2003. Epicormic branches: A growth indicator for the tropical forest tree, Dicorynia guianensis Amshoff (Caesalpiniaceae). Annals of Botany 92: 97–105.
Nicolini, E., B. Chanson, AND F. Bonne. 2001. Stem growth and epicormic branch formation in understorey beech trees (Fagus sylvatica L.). Annals of Botany 87: 737–750.
Passo, A., J. Puntieri, AND D. Barthélémy. 2002. Trunk and main-branch development in Nothofagus pumilio (Nothofagaceae): A retrospective analysis of tree growth based on the size and structure of its annual shoots. Canadian Journal of Botany 80: 763–772.[CrossRef]
Primack, D., C. Imbres, R. B. Primack, A. J. Miller-Rushing, AND P. Del Tredici. 2004. Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. American Journal of Botany 91: 1260–1264.
Reich, P. B., AND R. Borchert. 1984. Water stress and phenology in a tropical dry forest in the lowlands of Costa Rica. Journal of Ecology 72: 61–71.[CrossRef][Web of Science]
Richards, P. W. 1996. The tropical rain forest, an ecological study. Cambridge University Press, Cambridge, UK.
Sabatier, D., AND H. Puig. 1986. Phénologie et saisonnalitéde la floraison et de la fructification en forêt guyanaise. Mémoire du Muséum d'Histoire Naturelle de Paris, Serie A, Zoologie. 132: 173–184.
Sakai, S. 2001. Phenological diversity in tropical forests. Population Ecology 43: 77–86.[CrossRef][Web of Science]
Saporta, G. 1990. Probabilités, analyse de données et statistique. Technip, Paris, France.
Shinozaki, K., K. Yoda, K. Hozumi, AND T. Kira. 1964. A quantitative analysis of plant form: The pipe model theory. I. Basic analyses. Journal of Ecology 14: 97–105.
Simpson, G. G., A. R. Gendall, AND C. Dean. 1999. When to switch to flowering. Annual Review of Cell and Developmental Biology 15: 519–550.[CrossRef][Web of Science][Medline]
Stevens, P. F. 2001 onward. Angiosperm phylogeny website, version 8 [more or less continuously updated], http://www.mobot.org/MOBOT/research/APweb/[accessed 13 August 2007].
Stevenson, P. R. 2006. Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia. Primates 47: 239–247.[CrossRef][Medline]
Stevenson, P. R., M. J. Quiñones, AND J. A. Ahumada. 1998. Annual variation in fruiting pattern using two different methods in a lowland tropical forest at Tinigua Park, Colombia. Biotropica 30: 129–134.[CrossRef][Web of Science]
Van Schaik, C. P., J. W. Terborgh, AND S. J. Wright. 1993. The phenology of tropical forests: Adaptative significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24: 353–377.[Web of Science]
Vázquez-Yanes, C. 1980. Notas sobre la autoecología de los árboles pioneros de rápido crecimento de la selva tropical lluviosa. Tropical Ecology 21: 103–112.
Wallace, R. B., AND R. L. E. Painter. 2002. Phenological patterns in a southern Amazonian tropical forest: Implications for sustainable management. Forest Ecology and Management 160: 19–33.[CrossRef][Web of Science]
Wheeler, W. M. 1942. Studies on neotropical ant–plants and their ants. Bulletin of the Museum of Comparative Zoology 90: 1–162.
Whitmore, T. C. 1998. An introduction to tropical rain forests. Clarendon Press, Oxford, UK.
Zimmermann, M. H. 1983. Xylem structure and the ascent of sap. Springer-Verlag, Berlin, Germany.
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