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Ann Bot. 2009 November; 104(6): 1183–1194.
Published online 2009 September 11. doi:  10.1093/aob/mcp216
PMCID: PMC2766206

Phenology, growth and physiological adjustments of oil palm (Elaeis guineensis) to sink limitation induced by fruit pruning

Abstract

Background and Aims

Despite its simple architecture and small phenotypic plasticity, oil palm has complex phenology and source–sink interactions. Phytomers appear in regular succession but their development takes years, involving long lag periods between environmental influences and their effects on sinks. Plant adjustments to resulting source–sink imbalances are poorly understood. This study investigated oil palm adjustments to imbalances caused by severe fruit pruning.

Methods

An experiment with two treatments (control and complete fruit pruning) during 22 months in 2006–2008) and six replications per treatment was conducted in Indonesia. Phenology, growth of above-ground vegetative and reproductive organs, leaf morphology, inflorescence sex differentiation, dynamics of non-structural carbohydrate reserves and light-saturated net photosynthesis (Amax) were monitored.

Key Results

Artificial sink limitation by complete fruit pruning accelerated development rate, resulting in higher phytomer, leaf and inflorescence numbers. Leaf size and morphology remained unchanged. Complete fruit pruning also suppressed the abortion of male inflorescences, estimated to be triggered at about 16 months before bunch maturity. The number of female inflorescences increased after an estimated lag of 24–26 months, corresponding to time from sex differentiation to bunch maturity. The most important adjustment process was increased assimilate storage in the stem, attaining nearly 50 % of dry weight in the stem top, mainly as starch, whereas glucose, which in controls was the most abundant non-structural carbohydrate stored in oil palm, decreased.

Conclusions

The development rate of oil palm is in part controlled by source–sink relationships. Although increased rate of development and proportion of female inflorescences constituted observed adjustments to sink limitation, the low plasticity of plant architecture (constant leaf size, absence of branching) limited compensatory growth. Non-structural carbohydrate storage was thus the main adjustment process.

Key words: Carbon allocation, non-structural carbohydrates, source–sink relationships, Elaeis guineensis, phenotypic plasticity, photosynthesis

INTRODUCTION

Assimilate partitioning among growing organs is a function of active sinks in the plant (Marcelis, 1996; Heuvelink, 1997). Yield can thus be limited by the capacity of reproductive sinks, either in absolute terms or relative to the strength of competing, vegetative sinks. For oil palm, Elaeis guineensis, Henson (2006b, 2007), reported that vegetative growth and development constitute priority sinks that are comparatively invariable due to the low architectural plasticity of this species, whereas fruit production is more plastic and able to adjust to available resources. This type of behaviour was confirmed for coconut (Mialet-Serra et al., 2008), a plant that is taxonomically close to oil palm.

Oil palm has a simple, mono-axial shoot architecture that produces phytomers in regular succession. Each phytomer produces a single leaf and a male or female inflorescence. The development periods of both organs are long, up to 50 months for leaves (Henry, 1955) and up to 40 months for inflorescences (Corley, 1977). Consequently, adjustments of sexual (male or female) differentiation and probability of abortion of inflorescences on a given phytomer are determined between months and years before fruit filling, the main period of reproductive sink activity (Corley, 1977; Dufour et al., 1988; Gerritsma, 1988; Corley and Tinker, 2003a). Among the environmental factors that have been related to sexual differentiation and abortion processes are photoperiod, drought (Ochs and Daniel, 1976; Dufour et al., 1988; Caliman and Southworth, 1998; Nouy et al., 1999), and unfavourable conditions for carbon assimilation in general such as leaf diseases (Ng, 1977; Corley and Tinker, 2003b) or artificial defoliation (Corley and Tinker, 2003a). Oil palm is characterized by long lag periods between a given environmental influence and its effect on the reproductive sink. Consequently, the phenological adjustments of the reproductive apparatus do not necessarily prevent source–sink disequilibria and may even contribute to discrepancies between available resources and demand.

The concept of oil palm being a plant whose rigid architecture is compensated by highly plastic reproductive development is probably insufficient to explain how the plant maintains its physiological equilibrium. For coconut, where the problem is similar, three mechanisms (Mialet-Serra et al., 2008) have been suggested to serve as buffer for transitory source–sink imbalances: (1) variable partitioning to roots; (2) variation in radiation use efficiency (RUE) through regulated photosynthetic rates (Iglesias et al., 2002; Dingkuhn et al., 2007) or respiration rate (Hrubec et al., 1985; Musgrave et al., 1986; Whitehead et al., 2004) or both; and (3) a large and variable reserve compartment for carbohydrates located in the stem (Mialet-Serra et al., 2005, 2008; Silpi et al., 2007).

The objective of this study was to analyse oil palm adjustments to an artificial sink limitation induced by continuous pruning of male and female inflorescences upon their appearance. Such a treatment can be expected to decrease significantly the overall sink activity in the plant because under non-pruned conditions, the reproductive sink absorbs about 45 % of dry matter produced (representing the crop's harvest index), or even more in energy terms because the fruits are rich in lipids. Specifically, the aim was to evaluate responses of dry matter partitioning among above-ground organs, leaf photosynthesis and non-structural carbohydrate (NSC) storage in the stem in order to identify the pruned plant's mechanisms affected in a situation of source–sink imbalance that may result from a temporary reduction in demand for assimilates.

MATERIALS AND METHODS

Experimental site

The study was carried out on an experimental plantation of the SMART Research Institute (SMARTRI, Smart Tbk.) located in Kandista Estate (Riau province, Sumatra Island, Indonesia, 0°55′0′'N, 101°21′0′'E, 100 m a.s.l.).

The site has a tropical humid climate. The rainy season occurs between November and January, with a monthly mean rainfall of 240 mm month−1 (averages from 1993 to 2005), and a drier season from June to August, with a monthly mean rainfall of 140 mm month−1 (averages from 1993 to 2005). Mean daily global radiation during the dry season (wet season) is 18·9 MJ m−2 d−1 (16·9 MJ m−2 d−1). Mean air temperature is 27·4 °C (27·0 °C), mean relative humidity is 79·0 % (81·1 %), mean vapour pressure deficit is 0·98 kPa (0·84 kPa) and mean evapotranspiration (Penman-Monteith) is 4·5 mm (3·9 mm).

The beginning of the experimental period (July 2006 to May 2008), was characterized by a 2-month dry spell (July and August 2006), followed by abundant rainfall (Fig. 1). Annual rainfall was 1613 mm in 2006 and 2001 mm in 2007. The other climatic parameters (mean temperature, incident photosynthetically active radiation, vapour pressure deficit), during this period were similar to the average recorded for the previous 12 years.

Fig. 1
Time courses of environmental parameters from January 2006 to May 2008. Top: mean monthly of air temperature and incident photosynthetically active radiation (PARi). Bottom: mean monthly vapour pressure deficit (VPD) and mean monthly rainfall at the SMART ...

To evaluate drought extent, climatic water balance (CWB) was calculated as rainfall minus potential evapotranspiration. CWB is commonly used as indicator for the length of growing period in agro-ecological zoning for rainfed systems (FAO, 1996). Potential evapotranspiration (mm month−1) was calculated according FAO guidelines (Allen et al., 1998).

The soil was predominantly sandy (78·0 % sand, 11·1 % silt and 10·8 % clay) of homogeneous texture and >3 m deep. Soil water content values at field capacity (pF 2·5) and wilting point (pF 4·2) were 0·17 and 0·06 m3 m−3, respectively.

Plant material

The genotype of Elaeis guineensis Jacq. used, called 63, was a high-yielding tenera hybrid resulting from a cross between a plant of dura deli origin (fruits with thin mesocarp, thick endocarp and large kernel) and one of pisifera avros origin (fruits with thick mesocarp, thin endocarp and small kernel) varieties.

Experimental design

The experimental plot was part of a larger, long-term genetic experiment covering about 30 ha. Planting density was 136 plants ha−1 in a 9·5-m equilateral, triangular pattern. Plants were 13 years old at the onset of the study (July 2006). The experiment took advantage of the replicated block design already in place. Fertilization was managed according to leaflet nutrient contents which is general practice in oil palm cultivation.

Treatment

The aim of the fruit pruning treatment (FPT) was to change source–sink relationships by eliminating the reproductive sinks. All male and female inflorescences were systematically removed before anthesis, preventing fruit set. Treatment started in July 2006. Six palms (i.e. six replicates) per treatment, located sufficiently far from the plot border to avoid border effects, were selected randomly.

Stem growth rate

Oil palm stems have no secondary growth and therefore have roughly constant diameter but variable height due to production of new phytomers at the stem top. Stem dry mass growth (kgDM month−1) rate was assumed to consist of three components: (1) height increase due to addition of stem segments associated with apical production of new phytomers (irreversible process); (2) density increase due to lignification as stem tissues age (irreversible); and (3) mass increase or decrease due to carbohydrate reserve storage or mobilization (reversible).

Apical stem mass growth was estimated from the stem height increment per month (number of new phytomers × internode length per phytomer), stem diameter and the empirical density of newly formed wood (dry mass : wet volume ratio equal to 0·10 g cm−3). The dry mass increment of existing stem parts were assumed to undergo a gradual weight increase due to lignification equal to 0·00074 g cm−3 month−1 (Corley and Tinker, 2003a). Changes in stem dry weight caused by changes in total NSC (monosaccharides + sucrose + starch) content were calculated on the basis of soluble sugar and starch concentrations measured regularly at four stem heights as described below.

Leaf growth rate

The total number of fully expanded leaves, newly appeared leaves and pruned or broken leaves were recorded twice a month from July 2006 onwards. The youngest fully expanded leaf in the top of the leaf crown was assigned as rank 1, the next leaf down as rank 2, and so on. The morphology of each pruned leaf was described when leaves (overall on a rank greater than 34) were pruned to facilitate inflorescence pruning or bunch harvest. On each pruned leaf, leaflets were counted. To measure the dry mass of the petiole, rachis and the leaflets, first the dry matter content of the petiole, rachis and leaflets was estimated by weighing sub-samples of each organ after drying at 104 °C. The time-course of monthly dry mass increment of each new leaf produced was assumed to follow a linear function (the function being fixed to fit the final mass of each pruned leaf) over 3 months after its appearance (on rank 1), corresponding to time of a rapid growth. To estimate the aggregate dry mass growth rates for new leaves growing during a given month, the monthly dry mass increments were calculated for all such leaves on the plant.

Inflorescence appearance rate

Inflorescences can be female, male or early aborted. Upon their appearance (i.e. the spathe opening or anthesis date), their type was recorded. For controls, bunch maturity date (i.e. harvest date for female inflorescence only) was noted. The numbers of fertilized and unfertilized fruits per harvested bunch were recorded; dry mass of the harvested bunch stalk, the spikelets and the two major fruit compartments (mesocarp and nut composed of endocarp and kernel) and oil : mesocarp dry mass ratio were measured. The time-course of monthly dry mass increment (kgDM month−1) of each harvested bunch was assumed to follow a linear function (forced with the final mass of the harvested bunch) over 10 months, corresponding to the period of rapid growth ending with maturity (i.e. harvest). To estimate the aggregate dry mass growth rates for all bunches growing during a given month, the monthly dry mass increments were calculated for each of them.

Photosynthesis measurements

Leaf gas exchange measurements were made regularly between July and November 2006 and between May and September 2007. In both cases, sampled leaves were fully expanded and mature [leaves between ranks 14 and 18, counted from the youngest fully expanded leaf (rank 1) in the top of the leaf crown] and leaflets located at the three-quarters position on the rachis. One leaf per plant and one leaflet per leaf were sampled daily. Each set of plant replicates was observed during two consecutive days during two consecutive weeks every 2 months. During a day, two sets of measurement were done, in the morning (0900–1200 h) and in the afternoon (1400–1600 h). Measurements of leaf gas exchanges were conducted with a portable IRGA (LCA-4; Analytical Development Co., Bio Scientific Ltd, Hoddesdon, Herts., UK) to determine light-saturated net photosynthesis (Amax). Measurements were made with a broadleaf chamber (6·25 cm2) and an integrated light source (ADDA, DC Brushless). The conditions in the cuvette were saturating irradiance (1200 µmol photon m−2 s−1; Dufrêne, 1989), constant temperature (30 °C), relative humidity (65–70 %) and air CO2 concentration (360 ppm). Leaf temperature was measured with a thermocouple inside the cuvette of the LCA-4. The leaflet was placed in the cuvette 1·5 min before the first recording. Three recordings were done at 1-min intervals.

NSC and leaflet nitrogen analyses

Two different sampling procedures were used to follow: (1) seasonal variations of NSC concentrations in the stem; and (2) NSC and nitrogen concentrations in the leaflets linked to Amax variations. Sampling for NSC analyses used similar methods as those described previously on coconut (Mialet-Serra et al., 2008).

For the first sampling, observations were made every 2 months for a period of 22 months (July 2006 to May 2008). Samples were generally taken in the morning, a procedure that took several days and 2 h per day. On the stem, radial core samples were taken using a Pressler drill (6·6 mm × 300 mm; Haglöf, Sweden). The stem samples (one or two cores) were collected at four heights (at each quarter of the stem from the ground to the base of the lowest leaf of the crown).

For the second one, leaflets close to the leaflet used for photosynthesis measurement were harvested three times a day (morning, midday and afternoon) on each replicate plant, between July and November 2006 and between May and September 2007.

In both procedures, sampled cores were placed in an ice box until further processing in the laboratory. The biochemical method used in the laboratory for sugar analysis was based on high performance liquid chromatography and was reported in detail by Mialet-Serra et al. (2005).

Total nitrogen concentration in the leaflets was determined after dry combustion following the Dumas method (Edeling, 1968).

Statistical analysis

First, a one-way analysis of variance (ANOVA using Statistix, version 8·1; Tallahassee, FL, USA) was performed to evaluate the effect of treatments (control and FPT) on plant structure and growth parameters (Table 1), NSC concentrations in the stem (Table 2), photosynthesis and leaflet NSC and nitrogen concentrations for each treatment (Table 3). Secondly, a two-way analysis of variance was performed to evaluate interactions between treatments and seasons on photosynthesis and leaflet NSC and nitrogen concentrations (Table 3). In both cases, multiple mean comparisons were made by the Tukey test and considered significant at P < 0·05.

Table 1.
Mean stem height at the end of the observation period in May 2008, mean stem height growth, canopy structure and mean phyllochron duration for the experimental period (July 2006 to May 2008) of control and fruit-pruned (FPT) palm trees
Table 2.
Mean glucose, starch and total non-structural carbohydrate (NSC) concentrations at four stem heights (at each quarter of the stem from the ground to the top of the stem, below the lowest leaf) of control and fruit-pruned (FPT) palm trees, 12 months (July ...
Table 3.
Mean light-saturated net CO2 assimilation (Amax), mean non-structural carbohydrate [glucose, sucrose, starch and total (NSC)] and mean nitrogen concentrations in leaflets for control and fruit-pruned (FPT) palm trees between July and November 2006 and ...

RESULTS

Canopy structure and morphology

The leaf area index (Table 1) was significantly higher (P < 0·01) for FPT (about 6 for FPT and 5 for controls) due to a shorter phyllochron (P < 0·01) resulting in a higher leaf number (P < 0·01) in this treatment. Leaflet number and rachis length, however, were extremely stable among phytomers between the two treatments, indicating that oil palm has low phenotypic plasticity for leaf morphology. Minimal and maximal observations did not differ by >6 % (leaflet number) or 5 % (rachis length) among approx. 40 subsequent phytomers (i.e. leaves) which appeared during the 22 months. Means of leaflet numbers for all leaves which appeared after application of the treatment were 405 for control and 402 for FPT. Leaflets had slightly but significantly (P < 0·01) lower specific leaf area and thus were probably thicker for FPT.

Vegetative and reproductive development rates

During the 22-month period of differential ablation treatment, stem height growth of FPT plants increased on average by 2·03 mm d−1 as compared with 1·73 mm d−1 for control plants, resulting in mean total stem height of 1171 cm for FPT and 1094 cm for controls at the end of the experiment (Table 1). Due to variability of stem height among replications, treatment effects were not statistically different.

Leaf appearance rate (phyllochron−1) significantly (P < 0·01) increased in FPT in the second month after treatment onset (Fig. 2A). This treatment effect remained nearly constant throughout the experiment. Time courses showed marked seasonal oscillations of unknown cause, the two treatments exhibiting strictly synchronous maxima and minima. The cumulative number of leaves appearing after treatment onset (Fig. 2B) was significantly (P < 0·05) greater in FPT than in controls from the 8th month onwards. The difference was highly significant (P < 0·01) after 14 months.

Fig. 2
(A) Time-courses of monthly frequency of new leaf appearance for control and fruit-pruned (FPT) palm trees for July 2006 to April 2008. (B) Cumulative number of new emitted leaves for control and fruit-pruned-treatment (FPT) palm trees for July 2006 to ...

The appearance rate of new inflorescences (Fig. 2C; anthesis as indicated by the opening of the spathe) was on average accelerated to the same extent as that of the appearance rate of new leaves, but in contrast to leaf appearance, dynamics of inflorescence appearance were not synchronous between FPT and controls. For controls, strong seasonal fluctuations of inflorescence appearance rates (between 1·2 and 2·5 month−1) were observed with maxima occurring in March–April and July–August. For FPT, appearance rates were initially reduced, then increased sharply on the 3rd and 4th month of treatment and remained high and comparatively stable thereafter. Fruit pruning thus did not only increase inflorescence appearance rate on average, but also suppressed much of its seasonal variation.

Vegetative and reproductive growth rates

Treatment effect on above-ground, vegetative dry matter gain (leaves and stem, including structural growth and reserves) became significant (P < 0·05) during the second month after ablation treatment onset (Fig. 3A) and remained positive during most months thereafter. The mean monthly increase was 4·9 kg plant−1 or 48·5 % greater than the control mean. Time courses of vegetative growth of FPT plants closely followed those of controls, but at a higher level. A major peak in vegetative growth rate was observed for FPT in September–October 2007.

Fig. 3
(A) Growth rate of above-ground vegetative (leaves + stem) organs for control and fruit-pruned (FPT) palm trees for July 2006–April 2008. Values are means of six replicates. Arrows indicate the beginning of the treatment and bars indicate standard ...

Mean total above-ground dry matter production (Fig. 3B) was 18·4 kg plant−1 month−1 (30·0 t ha−1 year−1) for controls, and only 15·1 kg plant−1 month−1 for FPT, corresponding to a reduction by 18%. The absence of reproductive sinks in FPT was partly compensated by significantly (P < 0·01) increased growth of both leaves and stem. Partitioning of the incrementally produced above-ground dry matter to leaves, stem and fruits (Fig. 3C) was 0·45 for fruits, this being the mean harvest index observed during the 22-month observation period. Partitioning to leaves was 0·38 in controls and increased to 0·61 in FPT. Partitioning to stem was 0·17 in controls and increased to 0·39 in FPT.

Sex differentiation and abortion rate of inflorescences

The monthly frequency of female, male and aborted inflorescence appearance is presented in Fig. 4. Frequency of female inflorescences fluctuated strongly during the year preceding treatment onset, but was roughly synchronous between controls and FPT (Fig. 4A). Fruit pruning led to a marked acceleration and thus, de-synchronization of dynamics of appearance of female inflorescences, seasonal peaks and minima occurring earlier. From early 2008 onwards (approx. 18–20 months after FPT onset), the frequency of female inflorescences became continuously higher in FPT than in controls.

Fig. 4
Time courses of monthly appearance frequency (A) of female, (B) of male and (C) of aborted inflorescences for August 2006 to May 2008 for control and fruit-pruned (FPT) palm trees. Values are means of six replicates and bars indicate standard error of ...

Frequencies of male and aborted inflorescence appearance were not available before onset of FPT. The frequency of male inflorescences (Fig. 4B) fluctuated in both treatments and was on average higher for FPT than for controls (P > 0·05). The frequency of aborted inflorescences (Fig. 4C) was mostly lower than for fertile inflorescences, but for controls it showed a marked peak in May–August 2007, followed by a smaller peak around January. These peaks were absent for FPT which had low abortion frequency throughout.

Partitioning ratios of inflorescences among female, male and aborted types are presented in Fig. 5B and C, along with dynamics of the CWB (Fig. 5A). The two abortion peaks observed for controls can hypothetically be associated with two dry spells that happened about 10 months earlier. Abortions affected mainly male inflorescences.

Fig. 5
Time courses of monthly (A) climatic water balance (CWB = monthly rainfall – potential evapotranspiration) and fraction of each inflorescence type (female, male and aborted) for (B) control and (C) fruit-pruned-treatment (FPT) palm trees for August ...

NSCs in stem

A marked vertical gradient in NSC concentration and composition was observed on the stem (Table 2). In controls, total NSCs showed decreasing concentration from the top to the bottom. This gradient was mainly due to starch whereas glucose did not show a clear gradient. In FPT, the gradient was further amplified and starch accounted almost entirely for the increases in total NSCs. Reserve accumulation in FPT thus resembled a gradual filling-up process of starch from top to bottom.

FPT caused a gradual and highly significant (P < 0·01) increase in total NSC concentrations [starch + soluble carbohydrates (glucose + fructose + sucrose)] in the top part of the stem (Fig. 6A) during the experimental period. This resulted in a 1·8-fold increase compared with the control in the course of 22 months, attaining values up to nearly 500 mg g−1. Not all NSCs participated in this increase; in FPT, glucose concentration consistently decreased whereas total NSC concentration strongly increased due to a strong increase of starch concentrations (data not shown). The observed seasonal fluctuations in glucose in controls, as opposed to the smoother dynamics in FPT, were not correlated with any physiological or morphological variable observed on the plant.

Fig. 6
(A) Time courses of non-structural carbohydrate (NSC = glucose + fructose + sucrose + starch) and glucose concentrations in the top of the stem for control and fruit-pruned (FPT) palm trees for July 2006 to April 2008. Values are means of six replicates ...

The relative contribution of individual carbohydrates to total carbohydrate reserves in stem top fluctuated strongly in controls (Fig. 6B). Starch and glucose were the dominant fractions, on average 79·3 and 76·9 mg g−1, followed by sucrose (45·7 mg g−1) and fructose (21·0 mg g−1). In FPT (Fig. 6C), the starch fraction increased and constituted more than two-thirds of the carbohydrate reserves at the end of the experiment, whereas the glucose fraction declined, and sucrose and fructose fractions remained about constant.

Leaf photosynthesis, leaflet NSC and nitrogen concentrations

Mean light-saturated net photosynthesis (Amax) of leaflets for 2006 and 2007 observations are presented in Table 3. Means of Amax for FPT were 14 % higher in 2006 and 7 % higher in 2007 but not significantly. This trend was possibly due to differences in lower specific leaf area (P < 0·01; Table 1), whereas leaflet total NSCs and glucose, sucrose, starch and nitrogen concentrations were unaffected by treatment (Table 3).

DISCUSSION

This study followed up on two previous studies, one investigating the phenotypic plasticity of coconut growth and development under experimentally imposed source–sink imbalances (Mialet-Serra et al., 2008) and the other investigating oil palm growth and development responses to naturally varying environments (Legros et al., 2009). The studies indicated that phenological and morphological adjustment processes in tropical palm crops occur with substantial lags in the order of months to years, due to long development periods of individual phytomers and organs (Henry, 1955; Corley and Gray, 1976) and to the mono-axial architectural rigidity of these plants (Corley et al., 1971; Henson, 1999, 2006a), particularly their vegetative architecture. In coconut, plants adjusted transitory source–sink imbalances in the short term with variable, apparently demand-driven RUE, and, in both species, in the long term through variable fruit load. The morphology and development rate of vegetative plant parts thereby remained remarkably unaffected in coconut (Mialet-Serra et al., 2008), whereas phyllochron and bulk leaf growth were sensitive to environment in oil palm (Legros et al., 2009).

Phenological and morphological plasticity of oil palm induced by sink limitation

The present study applied an artificial FPT to investigate oil palm adjustments to severe sink limitation. Some morphological plant characteristics, such as leaf size and leaflet number, were not at all affected by FPT, neither initially nor after 22 months. This characteristic of oil palm, previously observed by Siregar (2006), was also found for coconut (Mialet-Serra et al., 2008), but stands in contrast to many species because leaf size is generally considered to be resource dependent (van Staalduinen and Anten, 2005; Luquet et al., 2006; Gordon and Dejong, 2007). Older reports, however, observed variable frond length and weight on oil palm (Calvez, 1976; Corley and Hew, 1976a, b).

In contrast to leaf morphology, leaf appearance rate of oil palm was strongly modified (accelerated) by sink limitation in this study. This is not the case, or is much less so, for coconut (Mialet-Serra et al., 2008). The acceleration of phyllochron by sink limitation (and thus, luxurious assimilate supply) was found to last at least as long as FPT continued (22 months). If the treatment had only accelerated leaf appearance through enhanced elongation of developing leaves, this effect would have soon exhausted itself, unless the initiation and development of new leaves had been accelerated as well. It is therefore evident that sink limitation accelerated the entire developmental cascade of phytomer and leaf initiation, development and appearance. It is thus concluded that oil palm development is not only driven by thermal time (Ong, 1982) and slowed by physiological stresses (Bredas and Scuvie, 1960; Nouy et al., 1999), as observed in many monocotyledonous plants and particularly grasses (Wu et al., 1997), but is also driven by assimilate availability. Sink limitation accelerated the appearance of inflorescences (totals including female, male and aborted) on average to the same extent as it accelerated leaf appearance (Fig. 2).

Sex differentiation and inflorescence abortion

Under FPT, the frequency of female inflorescences appearance was markedly accelerated, an observation that is in accordance with the general acceleration of development rate observed for this treatment. It took 18–20 months of treatment, however, to induce a significant increase in female inflorescence number. This increase can be interpreted as a treatment effect on sex differentiation. Corley (1977), Dufour et al. (1988) and Caliman and Southworth (1998) estimated that sex determination happens about 24 months before anthesis, probably followed by a period of several months during which sex determination is reversible (Corley and Tinker, 2003a). Sex determination, or the resulting sex ratio, is environment dependent in oil palm; unfavourable conditions increasing the frequency of male inflorescences (Corley, 1977). In the present study, FPT increased available resources through sink limitation, as indicated by the continuous and strong increase in carbohydrate reserves. This was probably the cause of the immediate and sustained increase of phytomer and inflorescence development, the suppression of environment-induced abortions (lag period of around 10 months) and also of the greater numbers of female inflorescences (lag period of nearly 20 months).

The high but variable fraction of aborted inflorescences observed in controls in two instances appeared to be related to water deficit experienced about 10 months earlier. If this hypothesis is true, FPT, and thus luxurious assimilate availability, counteracted drought effects on abortion rate. Regardless of whether drought was the triggering factor for abortions in controls, it is certain that the trigger for the abortion peak did not happen >10 months before anthesis because the peak disappeared in FPT, a treatment that began around that time. This time lag for inflorescence abortion agrees with previous reports (Dufour et al., 1988; Caliman and Southworth, 1998). Corley (1976) reported that aborted inflorescences are predominantly female. In the present study, the opposite was observed because prevention of the two abortion peaks by FPT mainly increased the male fraction of inflorescences.

Physiological plasticity of oil palm induced by sink limitation

Legros et al. (2006) reported that about 65 % of plant carbohydrate reserves of oil palm are located in the stem, their largest overall fraction being glucose. Glucose accumulated along the entire stem, whereas starch accumulated at the stem top. Coconut shows a similar pattern, but in this palm the predominant soluble carbohydrate to accumulate along the entire stem is sucrose (Mialet-Serra et al., 2005). Reserve accumulation induced by FPT consisted entirely of starch and followed an acropetal gradient, whereas glucose concentration declined, particularly in tissues where starch accumulated. It thus seems that glucose and starch do not have the same function, and glucose may not serve a storage function at all despite concentrations attaining 100 mg g−1 in stem tops of controls (Fig. 6).

A major reservoir absorbing excess assimilates under FPT was NSC storage in the stem. The top part of the stem contained between 40 and 50 % reserves (soluble carbohydrates and starch confounded), associated with an increase in diameter of those parts of the trunk (data not shown). The nearly doubled stem mass growth observed for FPT (Fig. 3B) was to >80 % due to reserves, thus constituting the main pathway for the utilization of excess assimilates.

The FPT treatment created a pronounced and continuous sink limitation in the plant system, as indicated by accelerated organogenesis, increased above-ground vegetative growth and storage of reserves. Accelerated organogenesis, however, was insufficient to absorb the surplus of available assimilates, resulting in reduced overall growth. It appears that the extraordinarily low plasticity of organ size and the absence of branching in the vegetative architecture of oil palm limited the scope for major adjustments in partitioning of assimilates to new or enhanced, alternative sinks.

An unknown entity in this equation is the root system which inherently has greater plasticity than shoot architecture (Henson and Chai, 1997; Corley and Tinker, 2003a) and may have used some of the extra assimilates made available by fruit pruning. Daniel and Taffin (1974) have shown that fruit pruning in young oil palms stimulates global development of vegetative apparatus, in particular of fine roots. Mialet-Serra et al. (2008) quoted unpublished results (C. Jourdan, CIRAD, Montpellier, France) for coconut indicating positive effects of fruit pruning on root dry biomass (an increase of 30 % of root-system dry biomass, i.e. an increase of 25 kg per tree compared with 40 kg produced per year and per tree for the controls). In the present study, such an effect, if it took place, must be several times stronger to explain the observed FPT effects on RUE, as root growth would have doubled (1st year after FPT application) or tripled (2nd year after FPT application). It is thus possible that variable root growth accounted for some but not all of the variation in RUE (Mialet-Serra et al., 2008). Root-growth enhancing by FPT treatment would probably be limited to structural growth because the root system of oil palm (Legros et al., 2006) stores only a small amount of NSC reserves, constituting only 2 % of the total reserve pool.

Reserve carbohydrate pools are known to respond to source–sink imbalances (Jordan and Habib, 1996; Silpi et al., 2007). Models simulating phenotypic plasticity, such as EcoMeristem (Luquet et al., 2006), consider transitory reserves as a passive buffer of such imbalances, but Lacointe et al. (2004) and Silpi et al. (2007) reported that reserve formation in vegetative organs can constitute a sink in its own right, thus competing with other sinks. Mialet-Serra et al. (2008) reported that in coconut undergoing fruit ablation treatment, carbohydrate storage in stems constituted only a minor adjustment process to the sink limitation, whereas reduced overall growth explained a much larger part of plant response in quantitative terms. The physiological cause of decreased growth under nearly unchanged light interception was not known, but the authors speculated that leaf photosynthetic rates might have been smaller. In fact, many reports describe end-product inhibition of leaf photosynthesis, mediated by soluble carbohydrates, as a major adjustment mechanism to sink or transport limitation (Iglesias et al., 2002; Frank et al., 2006; Susiluoto et al., 2007). However, in the case of oil palm, no variation in light-saturated net photosynthesis (Amax) was observed. Leaflet NSC and nitrogen concentrations also did not vary between treatments. Consequently, feedbacks of plant demand for assimilate or an accumulation of NSCs in leaflets in oil palm were not plausible factors affecting growth in this study.

Conclusions

The aim of this study was to identify the adjustment processes to source–sink imbalances, and particularly sink limitation, which enable oil palm to maintain a state of equilibrium between assimilate production and utilization. The plant was found to adjust rapidly the rate of developmental processes to sink limitation, accelerating significantly the number of phytomers produced, including leaves and inflorescences. This response increased demand for assimilates and thus, represented an effective adjustment. No plasticity was observed, however, with regards to leaf size and leaflet number per leaf.

Sink limitation also suppressed the abortion of male inflorescences, estimated to be triggered at about 10 months before anthesis. It increased the number of female inflorescences produced, but only after an estimated lag of 20 months, approximately corresponding to the period of sex differentiation. This effect can also be considered as a positive adjustment to sink limitation because it increases assimilate demand for fruit filling, albeit with a delay that may render this adjustment ineffective in most situations, such as biophysical or biotic stresses of limited duration.

In quantitative terms, by far the most important adjustment process was increased starch storage in stems. This reservoir thus constitutes an important buffer for source–sink imbalances in oil palm. It remains unclear, however, why fruit ablation specifically increased starch storage but reduced glucose storage, glucose being the most abundant NSC reserve in oil palm when the fruit was not pruned.

These results, in combination with those presented in the precursor study (S. Legros et al., 2009) on the effects of natural environment variability on oil palm source–sink relationships and phenology will enable the development of a phenological and growth model for oil palm.

ACKNOWLEDGEMENTS

The authors would like to thank SMARTRI. We gratefully acknowledge the estate managers of Kandista for their logistic and technical support in the field, without which this study could not have been undertaken and, in particular, Ms Reni, Ms Rosna, Mr Rinto, Mr Pujianto and Mr Agus for their precious help in data collection, and Ms Ema and Mr Abdullah for carbohydrate analysis. Lastly, we wish to thank PT SMART Tbk. for funding of this study.

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