Nitrogen uptake by sago palm (Metroxylon sagu Rottb.) in the early growth stages

Abstract

Previous trials have revealed variable responses of sago palm (Metroxylon sagu Rottb.) to fertilizer application, particularly nitrogen (N). In the present study, we quantified the fertilizer use efficiency (FUE) of sago palm for the first time using ¹⁵N-labeled fertilizer in pot and field experiments. The pot experiment was conducted in Japan using a 2:1 mixture of sand to Philippine soil. The field experiment was conducted in Leyte in the Philippines. Both experiments consisted of three replicates in each of three treatments: control, ¹⁵N urea at 50 kg N ha⁻¹ and ¹⁵N urea at 100 kg N ha⁻¹. The N uptake of sago palm increased significantly, but inconsistently with increasing N application. The few instances of a significant increase in N uptake did not translate into significant improvements in growth parameters, except for the number of leaflets in the pot experiment. The FUE values for sago seedlings (< 6 months) in the pot experiment treated with 50 and 100 kg N ha⁻¹ were 10.5 and 13.2%, respectively, whereas for the 2-year-old sago palms in the field, the corresponding FUE values were 14.8 and 12.0%. The FUE values were similar at the two levels of N application in both experiments. Sago growth parameters appeared to be insensitive to N application, suggesting that the form of N and the timing of N fertilization are important factors for sago palms. Therefore, the use of N fertilizer in sago production can only be justified after determining and fully understanding the response of sago palm to N application.

Key words:

• fertilizer use efficiency
• growth parameters
• ¹⁵N urea
• Philippines
• sago palm

INTRODUCTION

Sago palm (Metroxylon sagu Rottb.) is considered to be a semi-wild crop because of its persistence and ability to grow on marginal soils. Sago leaves are used as a local source of roofing materials and the plant is of economic importance as a food source because of its ability to accumulate starch in its trunk (stem). Recently, attention has turned to finding new uses for sago starch, including in the manufacturing of alcohol, citric acid and bio-ethanol; the residues from starch extraction have also been used to make biodegradable plastics (Igura et al. 2007; Ohmi et al. 2003).

The starch productivity of sago palm varies with soil type. The average yield of dry starch has been reported to range between 88 and 179 kg per palm in peat soils and between 123 and 189 kg per palm in mineral soils of Sarawak, Malaysia (Sim and Ahmed 1991). Jong et al. (2006) reported that starch was accumulated progressively in the trunk of sago and that each palm was capable of producing approximately 200 kg of dry starch. At harvest time, the sago palm can reach a height of 25 m with a harvestable trunk of 8–16 m and a diameter of 40–70 cm (Flach 1980). Considering the high biomass production of sago palm, it follows that there should be concern over the depletion of soil nutrients. Therefore, the addition of fertilizer might be essential to compensate for the depleted nutrients. Although sago palms grow in Histosols (peat soils) as well as in mineral soils, the optimum growth conditions include intermittent flooding by water with a high nutrient content, regardless of the soil type (Flach 1983). Sago palms grow naturally in mineral soils along the creeks and streams of fresh water and marshlands in the Philippines (Loreto et al. 2006), and when cultivated their growth and development is highly dependent on the cultivar and the environmental conditions (Jong 1995).

Enhanced growth and more intensive cultivation are needed to cope with the demand for food from an increasing population. For sustainable production of sago palm, its nutrient requirements need be elucidated to increase productivity and shorten the maturity period of 8–12 years. However, very little information has been reported with regard to the response of sago palms to fertilization.

Previous fertilizer trials with sago have shown variable responses, particularly to nitrogen (N) fertilizer. Sago growth parameters, such as the rate of leaf (frond) production, diameter growth, height increase (Kueh 1995) and leaf formation (Purwanto et al. 2002) were not affected by N application. Watanabe et al. (2005) reported that neither the growth nor growth rate increased under 20 different fertilizer regimes. In contrast, Paquay et al. (1986) reported that increasing fertilizer levels using a standard liquid fertilizer resulted in faster leaf area growth per palm. In addition, they stated that at all fertilizer levels the application of extra N generally showed a positive effect on the growth and development of sago palm seedlings. Similarly, in a nutrient omission trial, palms cultured with N had a relatively consistent leaf emergence rate across the different treatments (Jong et al. 2007). Kimura et al. (2008) found that the growth rate of sago tended to be lower at a high fertilizer application rate (150 kg N ha⁻¹) and higher at a low fertilizer application rate (50 kg N ha⁻¹), particularly when applied in the form of a slow-release fertilizer. Purwanto et al. (2002) reported that the concentration of N in sago palm leaves increased with the level of soil-applied N. However, the actual N uptake efficiency of sago palm is still unknown.

The use of stable-isotope techniques is a common tool in nutrient dynamic studies, and is particularly useful for revealing the nutrient requirements of plants. For nitrogen, the most common method is to use fertilizers enriched with ¹⁵N. However, no studies of ¹⁵N uptake by sago palm have been published, so the N requirements and N use efficiency of applied fertilizer are unknown for sago. Intensive monitoring of the N uptake of sago palm requires a lengthy study period because the palm takes 12–17 years to attain maturity (flowering stage) on deep natural peat and 8–12 years when growing in mineral soils (Jong and Flach 1995; Yamaguchi et al. 1997). Hence, pot and field experiments were conducted to determine the N uptake of sago palm using a stable-isotope tracer at various early growth stages. The current study on the N uptake of sago palm using ¹⁵N isotopes is the first report to determine the nitrogen use efficiency of sago palm. The objective of the present study was to elucidate the N uptake efficiency of sago palm from applied fertilizer in pot and field experiments.

MATERIALS AND METHODS

Pot experiment

Establishment of the ¹⁵N fertilizer experiment

For the pot experiment, 2-month-old sago palm seedlings germinated in Leyte, in the Philippines, were transplanted in October 2006 into double-layered polyethylene pots. The inner pot had a diameter of 14 cm and a height of 17 cm. Seedlings were used instead of suckers because of the unavailability of sago palms in Japan.

The potting medium used was a mixture of sand and Philippine soil (Eutropepts) at a 2:1 w/w sand : soil ratio. Original soil samples were collected from a depth of 0–20 cm from the sago experimental field at Visayas State University (VSU), Leyte. The soil had a slightly acidic pH of 6.4, an electrical conductivity of 3.4 mS m⁻¹, total carbon of 8.8 g kg⁻¹ and total nitrogen of 0.9 g kg⁻¹ with 0.1 mg N kg⁻¹ in the form of NO^- ₃ and 1.6 mg N kg⁻¹ as NH⁺ ₄. The bulk density of the soil was 1.09 g cm⁻³ and the texture was silt loam.

We used three levels of fertilizer for the treatments: control (without N), 26 mg N per pot and 52 mg N per pot. These doses were equivalent to 50 and 100 kg N ha⁻¹, respectively, based on the surface area of the soil in the pots. The ¹⁵N-labeled urea was diluted at a 1:50 fertilizer : water ratio with deionized water and evenly distributed over the surface of the soil. The ¹⁵N-labelled urea used had 3.35 atom %. The treatments were designated as the control, 15N-50 and 15N-100 for the non-fertilized pots and ¹⁵N urea at 50 and 100 kg N ha⁻¹, respectively.

The total amount of ¹⁵N-labeled urea to be applied was divided into two applications, the first half was applied 2 weeks after planting and the other half was applied 1 month later. Watering was done whenever necessary and the amount of water was controlled to minimize leaching (simulating upland conditions). The experiment was conducted in a greenhouse at the Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Tokyo, Japan. The temperature was artificially controlled and kept between 20 and 25°C during the period of the experiment.

Sago growth parameters

The plant height (cm) was determined each month by measuring the height of the palm from the base to the tip of the tallest leaf. Growth rate was evaluated by calculating the monthly increase in height. In addition, the basal diameter of the plant stems was determined using a measuring tape, and the numbers of leaves and leaflets were counted each month. The experimental period was set at 6 months, but the sago palms were maintained for further less-intensive observations.

Nitrogen uptake by sago

To evaluate N uptake by the sago palms from the added fertilizer, one leaflet was analyzed from a recently fully expanded mature leaf of each plant every month. The leaflet was chosen to avoid bias and to standardize the physiological stage of the leaflet being sampled. Thus, every 2 months the leaflet sampling point changed from the present sampling leaf to a newly fully developed leaf with a differing size and number of leaflets.

Total N analysis was carried out using a CN corder (Yanagimoto MT-700; Yanaco, Tokyo, Japan). The ¹⁵N was determined by an elemental analyzer (Euro-EA-Elemental Analyzer; Eurovector, Milan, Italy) connected to a continuous flow isotope ratio mass spectrometer (Isoprime, GV, Manchester, UK). Leaflet samples were washed with deionized water, oven-dried for 2–3 days at 70°C using a forced-draft oven and ground with a ball mill (model MM 301; Retsch, Haan, Germany). The N uptake per palm was calculated as the product of N concentration in the leaflet (mg N g⁻¹ dry weight [DW]), the oven-dry weight per leaflet and the number of leaflets per palm. Fertilizer use efficiency (FUE) was calculated using:

(1)

where δ¹⁵N_lab is the ¹⁵N/¹⁴N ratio of the labeled plant, δ¹⁵N_con is the ¹⁵N/¹⁴N ratio of the control plant and δ¹⁵N_fert is the ¹⁵N/¹⁴N ratio of the fertilizer given (8146‰).

The N uptake and FUE results at 1, 3 and 5 months after ¹⁵N application are reported.

Field Experiment

Establishment of the ¹⁵N fertilizer experiment

The field experiment was conducted in an ongoing sago experimental field at VSU in the Philippines (10°45′10.7″N, 124°47′23.6″E). The Soil Map of the Philippines (Mariano and Valmidiano 1972 cited in Badayos 1994) shows that most of the arable soils in the Philippines are classified as Inceptisols, particularly Eutropepts (46.78%). The details of the soil chemical and physical properties were presented above.

Two-year-old sago palms that had been propagated from suckers and that were of nearly uniform height were selected for the ¹⁵N experiment, which commenced on 24 July 2007. Each plot was 8 m² (2 m × 4 m) and had been established in May 2005. The same treatments were used as in the pot experiment: control and ¹⁵N-labeled urea at two rates (50 and 100 kg N ha⁻¹). Three replicates were used for each treatment with one palm per plot, hence a total of nine palms were chosen for the ¹⁵N study. The plots in the field were laid out in a randomized complete block design. The ¹⁵N-labeled urea we used had 3.35 atom %. The ¹⁵N was applied at rates of 0.094 g per plot (50 kg N ha⁻¹) and 0.189 g per plot (100 kg N ha⁻¹) and positioned within an area of 0.5625 m² (0.75 m × 0.75 m) centered around the stem of each plant on 25 July 2007. The remaining amount of N needed per plot was supplied using common urea. This fertilizer was applied at a distance of 10 cm from the palm, and evenly distributed at a depth of 5 cm around the palm. Intermittent flooding was maintained throughout the period of the study. The nine sago palms were destructively sampled on 8 January 2008.

The experimental area has a Type IV climate (Food and Agriculture Organization 2008), that is, it is generally wet throughout the year with heavy rains occurring between November and February. The total amount of precipitation over the period of the experiment was 2,120 mm, as measured by the Agro-Meteorological Station of the VSU campus, Baybay, Leyte. This was slightly less than the average for the preceding 10 years (2,996 mm). The highest monthly rainfall occurred in November 2007 (404.4 mm). The average minimum and maximum temperatures were 23.0°C and 30.9°C, respectively.

Sago growth parameters

In the field experiment, plant height was measured each month using a 12-m measuring pole (Senshin Kogyo, Glass Fiber; Senshin Industry, Osaka, Japan) and the number of leaves per palm was counted starting at 1 month after the ¹⁵N application and continuing for 6 months. The three replicates from each treatment (a total of nine sago palms) were destructively sampled at approximately 6 months after the ¹⁵N applications were initiated. Each palm was carefully excavated by shovel to capture all the roots. Large roots (≥ 5 mm) were separated from fine roots (≤ 5 mm) by hand. Meanwhile, another team removed the leaves from the trunk and weighed them and counted the number of leaflets per leaf. All above-ground biomass was recorded separately from the below-ground biomass (roots). The root : shoot ratio (R:S) was calculated by dividing the DW of the roots by the DW of the above-ground biomass. For comparison with the data from the pot experiment, only the cumulative increase in height, monthly growth rate, basal diameter, number of leaves and total number of leaflets are presented.

Nitrogen uptake by sago

To determine the N uptake, a recently fully expanded mature leaf (the third leaf from the top) of each sago palm was collected every month. The middle leaflets of the leaf were sampled in alternate months for the determination of total N uptake and ¹⁵N. In addition, the N concentration in leaves of different age was determined 6 months after N application. Leaflet samples from the middle part of young (upper leaf), intermediate (middle leaf) and mature (lower leaf) leaves were collected for N analysis. The details of the sample preparation, analyses and calculation of FUE were presented above.

Statistical analysis

Statistical analyses (one-way and two-way anovas) for all parameters in both experiments and Fisher's least significant difference tests were carried out using SigmaStat (SSI, Version 3.11; Systat Software, Point Richmond, CA, USA).

RESULTS

Sago growth parameters

The sago palms in the pot experiment grew 6.0–11.0 cm in the 6 months following N application (Table 1). Although some trends can be seen, N application resulted in statistically significant improvement in only one growth parameter, the number of leaflets per palm, in the pot experiment. The highest application rate (15N-100) resulted in significantly more leaflets than the other two treatments, whereas the control plants had the fewest leaflets, although the mean was not significantly different from that of the 15N-50 treatment.

In the field experiment, the cumulative increase in palm height ranged from 20.5 to 49.7 cm and the average growth rate ranged from 4.1 to 9.9 cm month⁻¹ (Table 1). The sago palms to which 100 kg N ha⁻¹ was applied tended to be superior in the field; however, the data were variable and none of the treatments were significantly different from the others for any parameter. It is worthwhile mentioning that the basal diameter of the sago palm, which is an important organ for accumulating starch, showed no indication of any difference among treatments in either experiment.

Nitrogen uptake by sago

The dry weight, N concentration (mg N g⁻¹ DW) and total N uptake (g N per palm) of leaflets in the pot experiment for 3-monthly measurements after the initial treatment are presented in Table 2. During each investigated month, there were no significant differences among the treatments for leaflet weight or N concentration at each month. The decrease in N concentration from the first month to the fifth month in the 15N-50 treatment was not statistically significant. For N uptake in the pot experiment, there was a significant treatment effect in the first and fifth months after fertilizer application (Table 2). During the first month, the 15N-100 treatment revealed an N uptake of 0.40 g N per palm, which was double the values (and significantly higher) recorded in the other two treatments (Table 2). However, the trend in N uptake across treatments changed in the fifth month, with the control having a significantly higher N uptake than the 15N-50 treatment and a comparable uptake to the 15N-100 treatment.

Table 1 Growth parameters (mean) of sago at various growth stages as influenced by N fertilization in the pot and field experiments at 6 months after N fertilization

Treatment	Cumulative increase in height (cm)	Monthly growth rate^† (cm)	Base diameter (cm)	No. leaves per palm	No. leaflets per palm
Pot experiment
Control	11.0 ± 0.2	1.8 ± 0.7	7.4 ± 0.5	6.3 ± 0.6	15.0 ± 3.5 b
15N-50	8.0 ± 1.2	1.5 ± 0.5	6.3 ± 1.7	6.0 ± 1.0	20.3 ± 3.1 b
15N-100	6.0 ± 0.5	1.0 ± 0.6	7.2 ± 0.6	7.0 ± 0.0	23.0 ± 2.0 a
Field experiment
Control	20.5 ± 35.0	4.1 ± 7.0	64.3 ± 10.0	17.0 ± 1.0	398.0 ± 71.4
15N-50	38.3 ± 14.6	7.7 ± 2.9	60.7 ± 9.4	15.3 ± 0.6	331.3 ± 6.4
15N-100	49.7 ± 7.1	9.9 ± 1.4	62.3 ± 9.6	17.7 ± 2.5	453.3 ± 73.5
^†Growth rate was based on height. Mean ± standard deviation (n = 3 in both the pot and field experiments). Means with different letters are significantly different (P ≤ 0.05; Fisher's least significant difference test). 15N-50, ^15N urea at 50 kg N ha^−1; 15N-100, ^15N urea at 100 kg N ha^−1.

Table 2 Dry weight of leaflets, N concentration in leaflets and N uptake by sago in the pot experiment at 1, 3 and 5 months after N fertilization

Treatment	Month after N fertilization
	First	Third	Fifth	Mean
	Dry weight (g) of leaflets for N analysis
Control	0.14 ± 0.04	0.10 ± 0.02	0.12 ± 0.01	0.12
15N-50	0.13 ± 0.05	0.11 ± 0.02	0.09 ± 0.02	0.11
15N-100	0.18 ± 0.02	0.11 ± 0.01	0.12 ± 0.01	0.14
	N concentration (mg N g^−1 DW)
Control	26.1 ± 0.9	22.6 ± 3.4	17.9 ± 3.9	22.2
15N-50	26.1 ± 2.6	25.5 ± 1.8	14.7 ± 2.7	22.1
15N-100	26.2 ± 1.5	22.4 ± 4.0	19.6 ± 3.4	22.7
	N uptake (g N palm^−1)
Control	0.2 ± 0.1 b	0.2 ± 0.1	0.4 ± 0.1 a	0.3
15N-50	0.2 ± 0.1 b	0.3 ± 0.1	0.2 ± 0.1 b	0.1
15N-100	0.4 ± 0.1 a	0.3 ± 0.1	0.4 ± 0.1 a	0.4
Mean ± standard deviation (n = 3). Means with different letters are significantly different (P ≤ 0.05; Fisher's least significant difference test). 15N-50, ^15N urea at 50 kg N ha^−1; 15N-100, ^15N urea at 100 kg N ha^−1.

Table 3 Dry weight of leaves, N concentration in the leaves and N uptake by sago in the field experiment at 1, 3 and 5 months after N fertilization

Treatment	Month after N fertilization
	First	Third	Fifth	Mean
	Dry weight (g) of leaves for N analysis
Control	51.5 ± 37.6	103.2 ± 65.2	108.3 ± 38.0	87.7
15N-50	27.4 ± 9.3	70.7 ± 34.8	76.5 ± 35.6	58.2
15N-100	44.5 ± 16.9	126.1 ± 69.0	116.9 ± 56.9	95.8
	N concentration (mg N g^−1 DW)
Control	18.6 ± 1.5 b	20.5 ± 1.2	20.2 ± 1.3	19.8
15N-50	22.3 ± 0.6 a	19.1 ± 1.5	20.7 ± 1.7	20.7
15N-100	19.5 ± 0.5 b	18.1 ± 1.8	22.2 ± 1.4	19.9
	N uptake (g N palm^−1)
Control	11.4 ± 8.7	29.6 ± 19.0	33.2 ± 8.5	24.7
15N-50	7.5 ± 3.0	16.5 ± 5.8	22.2 ± 8.4	15.3
15N-100	10.4 ± 5.9	43.5 ± 35.8	45.2 ± 30.8	33.0
Mean ± standard deviation (n = 3). Means with different letters are significantly different (P ≤ 0.05; Fisher's least significant difference test). 15N-50, ^15N urea at 50 kg N ha^−1; 15N-100, ^15N urea at 100 kg N ha^−1.

The dry weight, N concentration and N uptake of leaves selected for N analysis in the first, third and fifth months in the field experiment are presented in Table 3. During the first month, the N concentration of leaves was significantly higher in the 15N-50 treatment than in the other two treatments, which were not significantly different from each other. In the third and fifth months, no significant differences were noted for any of the parameters (Table 3).

The N concentration of young leaves in the field experiment showed a pronounced and significantly greater N concentration than mature leaves in all treatments (Fig. 1). Middle leaves were intermediate in N concentration and were not significantly different from either the more mature or less mature leaves. The leaf samples for N uptake were taken near the young leaf; therefore, the sampling point was representative of where N was mostly concentrated.

In contrast, among the sago parts, N was most likely be stored in the trunk and leaves, indicating that these are important organs and provide a source of N for new growth (Ruamrungsri et al. 2006), whereas fine and large roots contain lower N concentrations (Table 4). However, in our study there were no significant differences in N concentration among the treatments for any organ. Furthermore, the DW of the different sago parts was not affected by the N level (Table 4).

Figure 1  Nitrogen concentration (mg N g−1 dry weight [DW]) in leaves at different ages in 2-year-old sago as influenced by N fertilization. Means with different letters are significantly different using Fisher's least significant difference test (P < 0.01). 15N-50, 15N urea at 50 kg N ha−1; 15N-100, 15N urea at 100 kg N ha−1.

Table 4 Root : shoot, dry weight and N concentration n different parts of 2-year-old sago as influenced by N fertilization

Treatment	Root : shoot	Sago parts
		Leaves	Stem	Big roots	Fine roots
		Dry weight (kg)
Control	0.13 ± 0.1	4.00 ± 1.6	0.47 ± 0.5	0.58 ± 0.7	0.19 ± 0.3
15N-50	0.19 ± 0.1	3.16 ± 0.6	0.29 ± 0.2	0.56 ± 0.3	0.17 ± 0.2
15N-100	0.12 ± 0.1	5.72 ± 2.8	0.53 ± 2.8	0.42 ± 0.1	0.19 ± 0.2
		N concentration (mg N g^−1 DW)
Control		17.2 ± 1.6	26.1 ± 4.7	4.3 ± 0.8	6.5 ± 0.4
15N-50		17.8 ± 1.7	18.8 ± 8.0	5.2 ± 0.7	6.4 ± 1.3
15N-100		17.4 ± 2.9	13.0 ± 2.3	4.6 ± 0.1	8.1 ± 1.9
Mean ± standard deviation (n = 3). 15N-50, ^15N urea at 50 kg N ha^−1; 15N-100, ^15N urea at 100 kg N ha^−1.

Figure 2  Fertilizer use efficiency (% FUE) in the sago palm pot experiment. Error bars are the standard deviation (n = 3). 15N-50, 15N urea at 50 kg N ha−1; 15N-100, 15N urea at 100 kg N ha−1.

Nitrogen uptake by sago from the fertilizer

The FUE is the percentage of N from added fertilizer taken up by plants (as shown by Eq. 1). In the pot experiment, the FUE of sago increased continuously from less than 10% in the first month to approximately 20% in the fifth month (Fig. 2). The treatments did not differ significantly from each other in any month or over the whole period (data from all months pooled).

In the field experiment, the FUE at 1 month after N application was close to 5% for both fertilizer application treatments (Fig. 3). There was a significant (P < 0.05) increase in FUE from the first to the third months, to approximately 20% in both treatments (Fig. 3). At the fifth month, the FUE decreased again to approximately 15% in both treatments. The FUE of the two treatments was not significantly different at any measurement time.

DISCUSSION

Influence of fertilization on the plant growth parameters of sago

Figure 3  Fertilizer use efficiency (% FUE) in the sago palm field experiment. Error bars are the standard deviation (n = 3). 15N-50, 15N urea at 50 kg N ha−1; 15N-100, 15N urea at 100 kg N ha−1.

The application of fertilizer to semi-wild plants like sago palm is not a common practice. For example, in Malaysia where there are large sago plantations, the government prohibits the application of fertilizer to sago because of the possibility of leaching of the nutrients into nearby water bodies (A. H. Hassan, pers. comm., 2001). Hence, the optimum fertilizer dosage and method of application remain uncertain. Findings from previous fertilizer trials have demonstrated that sago shows no clear trends in its growth response to N application (Watanabe et al. 2005) or that sago palms exhibit only small responses to N application (Kimura et al. 2008). In the current study, the growth of 2-month-old sago palm seedlings was generally not affected by N application (Table 1). Unlike the study of Yoneta et al. (2006), in which a palm height of 115 cm was obtained after 1 year, which suggests that sago palm growth was not restricted by any limiting nutrients because sago seedlings were grown in plastic pots containing soil culture (subsurface Andisol with low organic matter and pumice) to which MagAMp K (Hyponex, Osaka, Japan) had been added, our result reveals a slightly shorter palm height of 50 cm in 6 months. In the present study, we detected very few significant effects of N fertilization on sago palm growth parameters and low FUE (Figs 1, 2). The low FUE could have resulted from the form and timing of N application, low demand for N by sago palms during early growth and an imbalance of soil nutrients (Marschner 1995). However, our experimental procedure did not examine any of these factors. Significant increases in leaflet number, particularly in the pot experiment, were associated with the highest N uptake in the 15N-100 treatment, despite the low FUE. This increased foliage production is consistent with the results of Havlin et al. (1999), who found that increasing the rates of N, and to a lesser extent P and K, to an optimum level will assure early and efficient leaf cover.

The application of N slightly improved the growth parameters of sago in the field experiment, but the increases were not significant. This is because of the highly variable response of sago palms to fertilization, and more replicates are required to gain more reliable estimates of the population. The important growth parameter of height increased slightly with N application in the field experiment. The results of the field experiment supported the assumption that sago palm growth might be enhanced by providing N in the form of chemical fertilizer. This is consistent with the empirical observation that sago growth is slower on low-nutrient peat soils than on mineral soils. On peat soils, trunk formation takes approximately 6 years to start and at least 12 years to reach maturity, whereas on mineral soils, the corresponding periods are 4.5 and 10 years (Jong and Flach 1995).

The lack of any clear response of sago to N application in our study and in other experiments does not imply that supplemental nutrients are not required (Kueh 1995). Observations of the growth parameters of sago over a longer time period as affected by the form and timing of N fertilizer are necessary to determine the effect of fertilizer application.

Influence of fertilization on N uptake by sago

The N output from the soil through uptake by sago palms in peat soil (shallow and deep peat) has been examined previously (Flach and Schuiling 1991; Jong and Flach 1995; Sim and Ahmed 1991; Yamaguchi 1998). Okazaki et al. (2002) presented a non-molecular N balance for a sago garden in Sarawak, taking into account all possible sources of N (e.g. precipitation, turnover and inflow of water) available for uptake by sago. They found that the estimated N removed from the harvested sago palms was high (0.11 t N ha⁻¹ year⁻¹), indicating that the residue from harvested sago palms should be returned to the soil or that fertilizer should be applied to reduce soil N depletion. The results of the present study revealed N concentrations in sago leaves ranging from 1.5 to 2.6% (equivalent to 15.0–26.0 mg N g⁻¹ DW) in seedlings (Table 2) and from 1.8 to 2.2% (equivalent to 18.0–22.0 mg N g⁻¹ DW) in 2-year-old plants after N application (Table 3). Sim and Ahmed (1991) showed that the N concentration ranged from 1.9 to 2.6% in 2-year-old sago, and this is consistent with our study. Although N did not limit the growth of sago in the current study, the range of N uptake with or without N application was comparable to the critical level of foliar N in coconut palms, which is 1.8–2.0% (Magat and Margate 1988; Reddy et al. 2002).

The sensitivity of nutrient application to detect growth responses is considered to be lower in perennial crops than in annual crops because the former might require a long time to react to the nutrient additions (Yost et al. 1999 cited by Ares et al. 2003). The effect of fertilizer application on N concentration in sago palm leaves was consistently not significant in the different growth stages of sago (Sim and Ahmed, 1991). Kueh (1995) found that foliar N level was unaffected by the application of ammonium sulfate. Therefore, previous findings demonstrate the low sensitivity of sago to N application, and this is in accordance with our results. The decrease in N uptake in the 15N-50 treatment and the significant increase in N uptake by the control in the fifth month of the pot experiment indicate that N application did not affect N uptake (Table 2). Knowing that the availability of N from easily soluble fertilizer is high at the time of application, the N might have been lost in subsequent months, resulting in N uptake in the 15N-100 plants similar to that in the control plants by the fifth month. Therefore, the interaction between the form and timing of fertilizer applications should be further examined to fully understand the response of sago to fertilization.

The N concentration data from different-aged leaves indicate that a proportion of the N taken up by the sago palms in the early period following fertilization was transferred to the rapidly growing young leaves (Fig. 1). This suggests that sago, like other crops, can translocate N from older leaves to younger leaves (Flach and Schuiling 1991).

Nitrogen use efficiency of sago

In the present study, the FUE of the applied N by the sago palms was quantified for the first time using ¹⁵N. The results revealed that young sago palms (≤ 1 year old) had an average FUE ranging from 10.5 to 13.2% during the first 5 months after N application (Fig. 1). The average FUE of slightly older (2 years old) sago palms varied from 12.0 to 14.8% (Fig. 2). These low values of FUE could be explained by several processes and factors affecting N uptake, including a low demand for N by sago palms at these particular growth stages, the morphological characteristics of the roots (Agren and Franklin 2003; Kelly et al. 2001) or the balance of nutrients in the soil system (Marschner 1995). Shrestha et al. (2007) reported beneficial interactions between sago palms and free-living microorganisms. Therefore, there is a possibility that aerobic nitrogen-fixing bacteria colonizing the sago palm contribute to its low FUE.

The N uptake efficiency of sago palm in the present study was either lower or comparable to the efficiencies that have been reported for other commercially grown palms. For example, an oil palm (Elaeis guineensis) had a 33.4% nitrogen use efficiency from urea-based NPK addition 7 months after fertilizer application (Bah and Rahman 2004). However, peach palm (Bactris gasipaes), which is grown for palmito (heart-of-palm), had an FUE of 13% (Dinkelmeyer et al. 2003). Chui et al. (1996) observed a lower N uptake (13.1 and 19.6% at 1 and 3 months, respectively, after ¹⁵N application) by mangroves (Kandelia candel). Likewise, Salifu and Timmer (2003) revealed that although fertilization promoted N uptake, recovery of ¹⁵N from young black spruce (Picea mariana) averaged 12–19%, indicating low fertilizer efficiency for young trees. These results show that the FUE of sago palm is comparable to that of other perennial crops. As a wild or semi-wild perennial, it follows that the response of sago palm to fertilizer application will be influenced by factors that suppress or enhance its sensitivity.

Unlike other types of cultivated plants, such as cereals, whose FUE is quite high, the FUE of sago palms is low. Like rice, sago palms need an intermittent supply of water for growth and development. The FUE of rice can be affected by water management. Our results indicate that N is not a requirement of sago during the early stages of growth and sago palms without N application showed superior growth in most parameters, despite an increase in N uptake for palms supplied with N. Matsumoto et al. (1998) suggested that sago palms have a lower demand for several nutrients than oil palms, and this is consistent with the low sensitivity of sago palms to N fertilizer application in our study and in previous studies. The low N uptake efficiency of sago should be considered when planning N fertilization, so that losses of large amounts of unutilized N can be avoided.

Conclusions

The low FUE values by sago palm obtained in the present study as determined by ¹⁵N should be considered when planning N fertilization to avoid losses of large amounts of unutilized N. There was no significant difference between FUE at different fertilizer rates (equivalent to 50 and 100 kg ha⁻¹) for either sago seedlings or 2-year-old plants grown from suckers. The results showed that even though sago palm is considered to be a semi-wild plant, it did take up N from the added fertilizer at low rates. However, the low FUE of sago palm might have been caused by other factors not examined in our study, such as the form and timing of N application, nutrient imbalances or the ability of the roots to take up nutrients. Further work is needed to determine what mechanisms control N uptake in the early stages of growth in the sago palm.

Nitrogen application did not significantly improve the growth parameters, except for the number of leaflets in the pot experiment. Sago growth parameters appeared to be insensitive to N application, suggesting that the form of N and the timing of N fertilization are important factors for sago palms. Therefore, the use of N fertilizer in sago production can only be justified after determining and fully understanding the response of sago palm to N application.

ACKNOWLEDGMENTS

The authors would like to thank Professor Ryunosuke Hamada for valuable comments on an early draft of this paper. Funding from the Tropical Bio-resources Research Fund of the Japanese Society for the Promotion of Science is gratefully acknowledged.