The most challenging issue which emerged, as knowledge of the Fiji sago palm, its status, and utilization was gained, revolved around the fundamental conservation approach which the recovery plan should adopt. Should there be a push for international listing as an endangered or critically endangered species, inclusion on Fiji's Endangered and Protected Species Act, a ban on commercial use, strict protection, and priority identification of sago-protected areas? Alternatively, were the conditions in Fiji less conducive to a top-down legislative/administrative approach and more conducive to a controlled stimulation of the market for thatch using sustainable harvesting methods, such that the landowners would become interested in maintaining the sago stands for their own commercial benefit? Landowners in Fiji are extremely powerful in respect of the resources on their land, and NFMV with the Sago Palm Recovery Plan Committee opted for the latter approach in the Recovery Plan.

The management recommendations in the recovery plan are categorized into five main groups as summarized below.

1. Public Awareness/Working with Communities

The priorities here were to work with the following stakeholders:

**Fig. 10.5** Fiji sago heart of palm substitute – peach palm (*Bactris gasipaes*) after the third successive annual stem harvest – 5 years after planting (Photo: NFMV)

The priorities here were:

**Fig. 10.6** Ex situ planting of Fiji Sago Palm in the Garrick Forest Reserve, Navua planted by NatureFiji-MareqetiViti members

### **10.6 Conservation Management: Achievements and Lessons Learned from the First 5 Years**

The first 5-year Fiji Sago Palm Species Recovery Plan (2010–2015 NFMV 2010) is currently being reviewed with the intention of producing another 5-year plan building on the achievements and lessons learned. Currently NFMV is seeking the resources to initiate a comprehensive review with all stakeholders.

Table 10.1 provides a summary of outcomes of the recovery plan during its 5-year implementation period.

Notable achievements include:

Summary of outcomes of the Fiji Sago Palm Species Recovery Plan (2010–2015) during its 5-year implementation period

(continued)

150

Recovery plan action

Planned outcome/

Achievements 2010–2015

Comment

**Fig. 10.7** The Culanuku community Fiji Sago Palm stand which has been sucessfully restored with the removal of invasive creepers and replanting

In conclusion, despite some notable successes, given the seriousness of the decline of the Fiji sago palm, the achievements can been viewed as mixed, while overall progress has been an insufficient response in the circumstances. In part, this is probably because the *project* is not owned or *mainstreamed* by government (which has not contributed funding); the administrative energy still remains with NFMV which has difficulties in resourcing a program with the necessary continuity.

### **References**

**Open Access** This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

### **Part IV Agricultural Botany of Sago Palm**

### **Chapter 11 Dry Matter Production as a Basis of Starch Production in Sago Palm**

### **Yoshinori Yamamoto**

**Abstract** The differences of starch productivity of sago palms among folk varieties (hereafter, varieties) are discussed from the viewpoint of dry matter production which has been rarely reported in sago palm, to provide basic knowledge to establish the cultivation methods of sago palm and to select varieties for new introduction and breeding of new varieties. The research was performed in Kendari, Southeast Sulawesi, Indonesia, to clarify the dry matter production and the factors related to it in the sago palm varieties with different starch yields. The results revealed that the varietal differences of starch yield of sago palm varieties, Molat (425 kg dry starch/ palm) and Rotan (142 kg in dry starch/palm), are mainly based on the biomass difference and not on the difference of matter distribution ratios to the harvesting part (trunk/pith). The biomass production in sago palm is closely related to the leaf area per plant, mainly determined by the leaf area per leaf compared to the number of leaves per plant. The leaflet width contributed most to the leaf area per leaf. I concluded that the leaf area in sago palm was the key factor to determine the starch yield and varietal differences of leaflet width should be paid attention to as an important character to determine the leaf area.

### **11.1 Introduction**

Sago palm is a clustering (soboliferous), perennial plant which accumulates large quantities of starch in the stem (trunk). This characteristic of sago palm gives it tolerance to various climatic conditions. It can grow in marginal land such as deep peat soil, high water table areas, etc. Besides the increase of production of major world starch crops, it is very important to evaluate and develop new starch crops to effectively meet the growing demand from the predicted population increase in this century. New starch sources can reduce hunger in the world and, moreover, help deal with the crop production problems brought about by climate change due to global warming.

Y. Yamamoto (\*)

Formerly, Faculty of Agriculture, Kochi University, Nankoku-shi, Kochi, Japan e-mail<EMAIL_ADDRESS>
The starch productivity of sago palm is affected by environmental conditions, cultivation and management methods, processing practices and harvesting stage, as well as variety (i.e., folk variety) (Yamamoto 2011). The amount of starch accumulated in the trunk varies greatly among regions and/or varieties (Yamamoto 2006, 2011). To precisely understand the regional and/or varietal differences of starch productivity among sago palms, it essentially needs to be researched from the viewpoint of dry matter production. However, limited research on dry matter production in sago palm has been done so far (Yatsugi 1977; Flach and Schuiling 1991; Kaneko et al. 1996; Yamamoto et al. 2014, 2016).

Starch yield of sago palm was analyzed according to biomass produced, biomass ratio of harvesting portion (pith), and the starch percentage in pith. Therefore, to calculate the starch yield, starch yield (dry starch) = biomass (dry weight) × pith dry weight/biomass (dry weight) × starch dry weight/pith dry weight. That is, the starch yield is determined by biomass, biomass distribution ratio to pith, and starch content in pith. As for biomass production, it is mainly determined by leaf area, photosynthetic rate, and growth duration.

This chapter discussed the dry matter production and the factors related to it in sago palm to clarify the differences in starch productivities in sago palm varieties.

### **11.2 Biomass Production and Related Factors in Sago Palm**

The main data described in this chapter were collected in Kendari, Southeast Sulawesi, Indonesia, from 1998 to 2000. In Kendari, measurements were made of the changes in total sugar and starch in the pith of three major varieties, with general and local names: Molat (*Roe*), Tuni (*Runggunmanu*), and Rotan (*Rui*), along with palm ages (Yamamoto et al. 2010). Based on the starch yield results, Molat and Rotan were chosen as the highest and lowest yielding varieties to compare the changes of each organ or part biomass weight of the shoot (aboveground part) and leaf area and leaf area-related characters. Thirteen Molat palms, 1–7 years after trunk formation (ATF), and nine Rotan palms, 1–7 years ATF, of different ages were sampled to determine their biomass and leaf area (Yamamoto et al. 2014, 2016).

### *11.2.1 Leaf Area*

The sago palm leaf is pinnate and compound, consisting of rachis, petiole, and many leaflets attached to the rachis. The size of each leaf part increases from the lower to the higher node until the trunk formation stage. The size of each part almost reaches a maximum value at about the trunk formation stage, and the size remains the same until flower bud formation stage. However, the size gradually decreases acropetally after the flower bud formation stage (Yamamoto 1998). Nakamura et al. (2009) developed a method to analyze the leaf area of sago palm based on studies of leaf and leaflet characters (Nakamura et al. 2004, 2005).

Leaf area per plant was compared between Molat and Rotan. The result showed a great difference in leaf area per plant between the two from the early stage after trunk formation. The leaf area of Molat increased linearly, but that of Rotan did not show a clear increase after trunk formation. Table 11.1 shows the leaf and leaflet characters (average values after trunk formation to harvesting) in both varieties. All of the values in the measured characters of leaf and leaflets were higher in Molat than in Rotan except specific leaf area (SLA), and the leaf areas per plant on the average after trunk formation and at harvesting stage were 2.0 and 2.9 times higher in Molat (269.5 and 439.0 m2 ) than in Rotan (139.1 and 150.0 m2 ), respectively. The difference in leaf area per plant was mainly caused by the difference in leaf area per leaf (Molat 17.5, Rotan 11.1 m2 ) compared with that in the number of leaves per plant (Molat 15.0, Rotan 12.5). The differences of leaf area per leaf by the regions and/or varieties were reported by Flach and Schuiling (1991). As for the leaflet characters which related to the leaf area per leaf, the difference in leaflet width (Molat 11.6, Rotan 8.7 cm) was the greatest, and it showed the closest relationship with the leaf area per leaf. Yamamoto (2016) reported the same relationships among the characters related to leaf and leaflet areas in the sago palm varieties around Lake Sentani near Jayapura, Papua, Indonesia.

### *11.2.2 Photosynthesis*

Sago palm is classified as C3 plant based on its leaflet anatomy (Nitta et al. 2005) and characteristics of photosynthesis (Uchida et al. 1990). Although the research on photosynthesis of sago palm is minimal, Flach (1977) and Uchida et al. (1990) reported that the maximum photosynthetic rate is 13–15 mg CO2/dm2 /h and 8–12 mg CO2/dm2 /h, respectively, by using young seedlings grown in pots. Moreover, Uchida et al. (1990) clarified that a sago palm leaf attained a maximum photosynthetic rate after 37–45 days of unfolding of the leaf and more than 50 % of the maximum photosynthetic rate was maintained for 70 days after the unfolding of the leaf. This implies the lateness of sago palm leaf to attain the maximum photosynthetic rate and to retard the photosynthetic rate compared to an annual plant (Uchida et al. 1990). Sago palm leaf shows the shade leaf characteristics because of the low light saturation point (5.3 μmol/m2 /s) (Uchida et al. 1990).

On the other hand, the photosynthetic rate of sago palm leaf after trunk formation growing in the field is higher than that of seedlings grown in pots, ranging from 25 to 27 mg CO2/dm2 /h (Miyazaki et al. 2007). The photosynthetic rate differences between seedling and plant after trunk formation might be brought about by the differences in leaflet thickness, chlorophyll content, stomata density, etc. (Miyazaki et al. 2007). Leaf thickness and chlorophyll content (SPAD value) increase from sucker transplanting or emergence to trunk formation stage (Yamamoto et al. 2006). Uchida et al. (1990) reported that the photosynthetic rate of sago palm seedling is strongly affected by the stomata density. Omori et al. (2000) clarified that the differences in stomatal density based on the position in leaflets and leaves changed with palm age, that is, it ranged from ca. 50/mm2 on the adaxial side and ca. 400/mm2 on

aValues at harvesting time the abaxial side in the seedling stage to ca. 120/mm2 and ca. 1000/mm2 after trunk formation stage, respectively.

Miyazaki et al. (2007) reported the differences of photosynthetic rate of sago palm varieties growing in Bogor, Kendari, and Jayapura (around Lake Sentani), but the differences were small. According to Miyazaki et al. (2007) and the reports of the small differences in stomatal density by Omori et al. (1999), along with the study of mineral element contents in leaflets (Yoshida et al. 2000), there may be a small difference in photosynthetic rates between the Molat and Rotan varieties.

### *11.2.3 Growth Duration*

The growth duration from sucker planting or emergence to flowering stage, that is, harvesting stage, varies greatly among varieties (Yamamoto 2011). The range of growth duration is from about 10 to 25 years (Yamamoto 1998, 2011). Moreover, the growth duration is affected by the soil types and soil nutrient conditions where the sago palms grow (Yamamoto 1998). The biomass of sago palm at harvesting stage is greatly influenced by the growth duration. Biomass production of early maturing varieties is lower than that of the late maturity varieties. Yamamoto (2011) reported that the difference in starch productivity was assumed to relate closely to the years to flowering, as reflected from the positive high correlation between the numbers of leaf scars and living leaves and the dry pith weight or starch yield.

The growth duration from trunk formation to harvesting was a little longer in Molat (7 years ATF) than in Rotan (5.5–7 years ATF); however, it was not very different (Table 11.2).

### *11.2.4 Biomass*

The shoot fresh and dry weights ranged from 600 to 3053 kg in Molat and from 479 to 1123 kg in Rotan for the fresh weight and from 104 to 1028 kg in Molat and from 86 to 425 kg in Rotan for the dry weight (Table 11.2) and increased exponentially with years ATF. The annual weight gains ATF were 357.8 kg/year in Molat and 92.5 kg/year in Rotan for the fresh weight and 144.3 kg/year in Molat and 46.5 kg/ year in Rotan for the dry weight, with 3.9 and 3.1 times higher values in Molat than in Rotan, respectively. The average shoot fresh and dry weights at the harvesting stage (three palms at 7 years ATF for Molat and three palms at 5.5–7 years ATF for Rotan) were 2781 and 986 kg for Molat and 1000 and 359 kg for Rotan.

The leaf dry weight of Molat ranged from 76 to 291 kg and increased exponentially with years ATF, while that of Rotan ranged from 62 to 107 kg; a significant change with years ATF was not observed (Table 11.2). The trunk dry weight in both varieties ranged from 29 to 746 kg in Molat and from 25 to 336 kg in Rotan and increased exponentially with years ATF. The average trunk dry weight at harvesting stage in Molat (721 kg) was 2.7 times higher than that in Rotan (267 kg) (Table 11.2).

**Table 11.2** Changes in dry weight of each part of shoot of sago palm varieties after trunk formation in Kendari, Southeast Sulawesi, Indonesia

a Years after trunk formation

b Petiole + leaf sheath. The palms shown in gray color are at harvesting stage Source: Yamamoto et al. (2016)

All the leaf components, leaflet, rachis, and petiole + leaf sheath, in Molat increased exponentially in dry weight with years ATF (Table 11.2). On the other hand, in Rotan, although that of rachis increased linearly, few changes were observed in the dry weights of leaflet and petiole + leaf sheath with years ATF. Among the leaf components, the dry weight of leaflet, rachis, and petiole + leaf sheath ranged from 24 to 107, 22 to 77, and 30 to 107 kg in Molat, respectively, and 22 to 40, 15 to 29, and 21 to 38 kg in Rotan, respectively, showing the higher dry weight in the order of petiole + leaf sheath ≒ leaflet > rachis in both varieties.

Exponential increases of the bark and pith dry weights with years ATF in Molat and Rotan were observed. The dry weights of bark and pith ranged from 11 to 153 kg and from 18 to 600 kg in Molat, respectively, and from 7 to 65 kg and 18 to 270 kg in Rotan, respectively, while showing a marked varietal difference after 4 years of trunk formation. The average bark and pith dry weight values at the harvesting stage in Molat (141 and 581 kg) were 2.6 and 2.7 times higher than that in Rotan (55 and 213 kg), respectively (Table 11.2).

### **11.3 Dry Matter Distribution Ratio to Each Part of Sago Palm**

Table 11.3 shows the dry weight ratio of each organ or part to the shoot weight of varieties Molat and Rotan based on the values in Table 11.2. In contrast to the dry weight differences of each organ or part between the two varieties, there were no

**Table 11.3** Changes in dry weight percentage of each part of shoot of sago palm varieties after trunk formation in Kendari, Southeast Sulawesi, Indonesia

a Years after trunk formation

b Petiole + leaf sheath. The palms shown in gray color are at harvesting stage

Source: Yamamoto et al. (2016)

clear varietal differences in the changes of dry weight ratio of each organ or part to the shoot weight. The leaf and trunk weight ratio conversely changed showing 70–75 and 30–25% at trunk formation stage and 25–30 and 75–70% at harvesting stage, respectively. The dry weight ratios were almost the same at 3–4 years after trunk formation; thereafter, the trunk ratio increased with years ATF, compared to the leaf ratio. These ratios at harvesting stage are similar to the results from sago palms growing in Sarawak, Malaysia (Flach and Schuiling 1991; Kaneko et al. 1996).

Moreover, the dry weight ratio of each part of leaf to the shoot dry weight decreased with years ATF. Petiole + leaf sheath dry weight decreased more rapidly than in the other two parts, due to the gradual shortening of the length with palm age (Yamamoto et al. 2014).

The dry weight ratio of bark in the trunk to the shoot dry weight in both varieties ranged from 10 to 20% and did not differ with palm age. On the other hand, the ratio of pith of both varieties ranged from 15–20% to 55–60% and increased with years ATF. The pith dry weight ratio at harvesting stage was about 60% in both varieties. This value is a little higher than that in sago palms grown in Sarawak, Malaysia (Kaneko et al. 1996). Moreover, the pith dry weight ratios to the trunk dry weights at the harvesting stage in both varieties were about 80%. These results compared closely with those reported by Yatsugi (1977).

### **11.4 Starch Content (Percentage) in Pith of Sago Palm**

Samples were collected from the sago palm varieties Molat, Tuni, and Rotan of various ages, each growing in research gardens. The age range of Molat palms was 1–10 years ATF, 1–8 years ATF for Tuni, and 1–7 years ATF for Rotan. Samples were collected from 18 Molat palms, 17 Tuni palms, and 14 Rotan palms. Of those, five Molat, four Tuni, and five Rotan palms were at the harvesting stage, which is characterized by flower bud formation and flowering (Yamamoto et al. 2010). Total sugar and starch content in the pith were analyzed following the method of Murayama et al. (1955).

The starch percentage (dry weight basis) in the pith in Rotan increased from 1 to 3 or 4 years ATF and in Molat and Tuni from 3 to 7 or 8 years ATF. The final starch percentage (at harvesting stage) was almost the same in the three varieties (60–70%; dry starch weight/dry pith weight × 100). The starch percentage in the pith of each variety showed a positive and negative significant correlation with the dry matter percentage and the total sugar percentage, respectively (Yamamoto 1998, 2006; Yamamoto et al. 2010).

### **11.5 Starch Yield and Its Related Factors of Sago Palm**

The starch yields of three major varieties at harvesting stage were higher, in descending order, of Molat (425 kg/palm) > Tuni (305 kg/palm) > Rotan (142 kg/palm) (Yamamoto et al. 2010). The starch yields of Molat and Tuni were 3.0 and 2.1 times higher than that

**Table 11.4** Starch yield and dry matter production characters related to the yield

a Lower trunk portion from the node of lowest living leaf, which part is actually harvested for starch extraction in sago palm-growing areas

b Values quoted from Yamamoto et al. (2010)

c Calculated from the pith dry weight and the average starch percentage

of Rotan. Table 11.4 shows the starch yield and dry matter production characters related to the yield of both varieties. The results showed that the difference in starch yield between Molat and Rotan was based on the differences in the shoot, trunk, and pith biomasses and not on the ratios of harvested part and starch percentage in the pith.

### **11.6 Conclusion**

Shoot biomass (aboveground part) of sago palm increased exponentially after trunk formation, and those at harvesting stage (flower bud formation-flowering stages) showed a greater difference between the varieties Molat and Rotan. The shoot biomass was mainly determined by the leaf area per plant, and it was primarily determined by the leaf area per leaf compared to the number of leaves. The differences in leaf area per leaf between the two varieties were closely related to the width of leaflet compared to the number of leaflet and leaflet length.

The dry weight ratio of each organ or part of sago palm shoot after trunk formation was not very different between the two varieties. The dry weight ratios of leaf and trunk to the shoot weight decreased and increased with aging, respectively, and the pith ratio of harvesting trunk was about 60%.

The starch yields of Molat were three times greater than that of Rotan, and the yield differences were mainly based on the differences in shoot biomass.

The results presented above reveal that varietal differences in dry matter production based on leaf area provide useful information to establish the best methods of cultivation of sago palm and the leaf and leaflet traits may be useful as a selection trait to breed new high-yielding varieties.

### **References**

**Open Access** This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

### **Chapter 12 Morphogenesis of Sago Palm**

### **Satoshi Nakamura**

**Abstract** Suckers are normally used for sago palm propagation. The stem of a transplanted sucker elongates in a horizontal direction on the ground, producing leaves in the first 4–5 years after transplanting (the rosette stage). During the rosette stage, transplanted suckers produce large numbers of daughter suckers which develop from lateral buds. The lateral bud of sago palm (sucker bud) differentiates on the opposite side of the axil. In the suckers for transplantation, detailed observation of the differentiation position and the development of the sucker bud showed that the sucker bud differentiates inside near the connate part of the leaf petiole. This is also the part that is gradually split as new leaves emerge and the stem enlarges. In the lower leaf position from rbL 6, which is the sixth leaf from the youngest leaf primordium, there were only one sucker bud and two sucker buds on leaf positions of 30.1% and 68.1%, respectively. Sago palm has reduplicate leaves; however, little has been reported on the leaf formation process of sago palm. The youngest visible leaf, a spear leaf, contains a number of folded leaflets and these open as the plant grows. Observation of the cross section of a spear leaf after trunk formation and the unemerged young leaves during rosette stage showed that the midribs of leaflet are on the adaxial side, and the edges of leaflet are on the abaxial side. When splitting occurs along the abaxial ribs, leaflets that are Λ-shaped in section form. These suggest that splitting would occur along the abaxial ribs in sago palm. An approximately 8-year observation of the stem length in the creeping part of transplanted suckers revealed that the creeping part length increased exponentially from transplantation to around 4 years, thereafter, and gradually increased slowly. As a result of growth analysis for creeping elongation of the sucker stem, the maximum elongation rate was estimated as 0.38 m per year at YAT 3.8.

S. Nakamura (\*)

School of Food Industrial Science, Miyagi University, Sendai, Japan e-mail<EMAIL_ADDRESS>
### **12.1 Introduction**

Sago palm (*Metroxylon sagu* Rottb.), which accumulates a large amount of starch in its trunk, is a hapaxanthic palm which dies after flowering. Generally, the suckers emerging from the base of stem are used for propagation. The stem of transplanted sucker elongates in a horizontal direction on the ground, producing leaves in the first 4–5 years after transplanting. During this period, called the *rosette stage*, the size of the leaves and stem increases gradually (Fig. 12.1a–c). After the rosette stage, the stem elongates from a horizontal direction to the vertical direction, swelling up at the bottom part with leaves attached (trunk formation), and the trunk (stem) then elongates vertically (Fig. 12.1d, e). The trunk is harvested during the time from just before flower initiation to flowering because the amount of starch accumulated in the trunk decreases thereafter due to the development of the inflorescence and fruit. Although the period for harvest differs by cultivated regions, varieties, and rate of growth, sago palm takes over 10 years from transplantation to the first harvestable trunk. In recent years, sago palm has received much attention as a starch crop for use not only as food but also an industrial raw material; however, the morphogenesis of sago palm is still incompletely understood. This chapter describes recent research on the suckers, leaves, and stem in the morphogenesis of sago palm.

### **12.2 Suckers**

Suckers are normally used for sago palm propagation (Sato et al. 1979). The suckers, cut from mature stems which are creeping horizontally, are grown as seedlings for about 6 months in a nursery and then transplanted into the field. During the rosette stage, transplanted suckers produce large numbers of daughter suckers which develop from lateral buds (Fig. 12.1b). In sago palm cultivation, thinning of daughter suckers in the clump is performed (sucker control) to regulate the density of the suckers. If all of daughter suckers grow well, the clump would become rampant with growth, and the suckers would have a negative influence on each other, resulting in reduction of starch productivity. Nabeya et al. (2013) reported that a farmer in Sarawak, Malaysia, not only has regulated the sucker density in the clump by pruning leaves of daughter suckers to suppress their growth but also has made observations of clumps consisting of suckers at different growing stages, the direction of the creeping growth, and the position of the trunk at harvest time. Yanagidate et al. (2009) suggested that proper cultivation techniques to maintain a suitable trunk density of different trunk lengths (ages) by appropriate sucker thinning should be established to achieve stable annual starch production per unit area, based on investigations in Southeast Sulawesi Province, Indonesia.

**Fig. 12.1** A sago palm without spines. (**a**) 1 year after transplantation (YAT 1), (**b**) YAT 2.9, (**c**) YAT 4.8, (**d**) YAT 5.8, and (**e**) YAT 7.8 in Sarawak, Malaysia. The *triangle* shows the transplanting position. The *arrow* indicates the position of the estimated growth point. The stem length in the creeping part was defined as the horizontal distance from the growth point judged by the appearance to the transplanting position. Bar = 50 cm (**a**, **e**), 1 m (**b**–**d**) (From Nabeya et al. 2015d)

### *12.2.1 Differentiation of Lateral Sucker Buds*

Although utilization and management of suckers are very important in sustainable sago palm cultivation, there are only a few reports about the presence and development of lateral buds from suckers. Goto et al. (1998) described how the lateral bud of sago palm (sucker bud) differentiates on the opposite side of the axil, unlike many plants. Fisher and Dransfield (1979) reported that the lateral bud of rattan palms *Daemonorops* spp. and *Korthalsia rigida* differentiated on the opposite side to the axil and named it a *leaf-opposed bud*.

Nabeya et al. (2015b) reported in detail the differentiation position and the development of the lateral bud of the sago palm sucker for transplantation. In sago palm, since the lower part of the petiole (leaf sheath) wraps around the stem, the part of

**Fig. 12.2** Connate part of both edge of the leaf petiole. (**a**) The connate part of the leaf petiole. (**b**) Sucker removed connate part of the leaf petiole presented in (**a**). The *triangle* denotes the reference point. Two sucker buds differentiated inside of the connate part of the leaf petiole and near the reference point. (**c**) A sucker bud greatly developed. Sucker bud (*A*) differentiated at the reference point and developed greatly. Sucker bud (*B*) differentiated at the position B′ and elongated narrowly. The *triangle* denotes the reference point. Bar = 10 mm (From Nabeya et al. 2015b)

the petiole attaching to the stem appears to be a node-like ring after removal of the petiole (Fig. 12.2a). At the connate part of the leaf petiole, following the vascular bundle along both edges of the petiole to the base, the two bundles fuse into one near the base. The sucker bud differentiates near the reference point which is inside the connate part of the leaf petiole (Fig. 12.2b). This is also the part that is gradually split as new leaves emerge and the stem enlarges. To investigate the differentiation of the sucker bud, the youngest leaf primordium, in which the tip of the hoodlike leaf was beyond the tip of growth point, was assumed to be rbL 1 (relative basipetally Leaf 1) and sequentially rbL 2, rbL 3, and so on (Nabeya et al. 2015b). Sucker buds which differentiated inside of rbL *n*, outside of rbL *n-1*, were regarded as rbS *n*. As a result of investigations, the sign of differentiation of rbS 1 and rbS 2 was not visible, but the swelling of tissue of rbS 3 and rbS 4 was visible in 13.6% and 77.3% of investigated suckers, respectively. The initiation of sucker bud of rbS 5 was visible in all of the investigated suckers; the sucker bud was visible in almost all of leaf position after rbL 5. In the lower leaf positions from rbL 6, only one sucker bud differentiated in a leaf position 30.1%, and there were two sucker buds and three sucker buds on leaf positions of 68.1% and 1.8%, respectively. In *Plectocomia elongata*, the instance of multiple vegetative buds differentiated in a leaf position was reported by Fisher and Dransfield (1979). In *P. elongata*, vegetative buds appear, one to ten, as small swellings in a node, and become multiple branches. By contrast, in sago palm, a small swelling occurred and then differentiated into two sucker buds (Nabeya et al. 2015b). An instance of both sucker buds developing and appearing from a leaf position has not yet been observed in our investigations.

### *12.2.2 Development of Sucker Buds*

It is not clear as to when and how sucker buds develop after differentiation and emerge from the leaf sheath. Nabeya et al. (2015b) reported that both the length and width of sucker buds from rbS 6 to rbS 13 increased exponentially in suckers for transplantation. In the lower leaf position from rbS 11, some sucker buds, greatly developed in length and width, were observed (Fig. 12.2c). The large sucker buds were about 7.0% of all sucker buds from rbS 11 to rbS 13, and the length and the width near the base were 28.7 ± 10.8 and 5.5 ± 2.0 mm on average, respectively. Some sucker buds that only increased in length but not in width were also observed from rbS 11 to rbS 13. Most of these sucker buds elongated in a meandering fashion like the one (B) shown in Fig. 12.2c.

A number of suckers emerge from the stem when it is elongating in a horizontal direction; however, few suckers emerge from the trunk, elongating in a vertical direction. Differentiation and development of sucker buds may be related to gravitational direction. Further studies are required to clarify the development and emergence of sucker buds.

### **12.3 Leaf**

The leaf, which is the distinguishing character of the palm, has three components: a sheathing base (a leaf sheath), a petiole, and a blade (Dransfield et al. 2008; Tomlinson 1990). Palm leaf blades are fundamentally of two types: pinnate or palmate (Dransfield et al. 2008). The sago palm has large compound pinnate leaves

which have many leaflets attached to an elongated rachis. The leaflets range in shape from linear lanceolate to narrow lanceolate. The leaf sheath is the extended base of the petiole, which wraps around the trunk and fuses on both ends (Fig. 12.2a). This fused state is observable from the leaf primordium stage, but no morphological boundaries between the petiole and leaf sheath are found on the adaxial or abaxial sides of the petiole (Goto and Nakamura 2004). The leaf sheath has two types: bearing spines on the abaxial surface of the petiole and spineless. The leaf sheath remains attached to the stem (trunk) after the leaf dies (Fig. 12.1c–e).

The youngest visible leaf, which has a pointed stick, forms and emerges along a groove running longitudinally in the petiole of the previous leaf and is called a spear leaf (Fig. 12.1a) (Jones 1995; Tomlinson 1990). A spear leaf contains a number of folded leaflets and these open as the plant grows. When a spear leaf opens, a cordlike tissue connects the tips of leaflets as if to trace the outline of the leaf and then falls away, or breaks up, leaving individual leaflets fully independent (Goto and Nakamura 2004). Sago palm reportedly has a phyllotaxis of 4/13 and a divergence angle of 110.77° (Jong 1991). Sago palm has a dextrorse or a sinistrorse phyllotaxis, depending on the plant.

### *12.3.1 Leaf Characteristics in the Rosette Stage*

Sago palm leaf size increases as the plant grows during the rosette stage (Fig. 12.1). Figure 12.3 exemplifies a sago palm 3.3 years after transplantation and leaf characteristics in the rosette stage (Nakamura et al. 2009). This plant has 16 leaves including a spear leaf and one dead leaf. The spear leaf provides a convenient marker for growth research. The position of the spear leaf, the emerging youngest leaf, is labeled as ebL 1, and the leaves thereafter are labeled basipetally as ebL 2, ebL3, and so on (Fig. 12.3a). Concerning the position of unemerged leaf, the leaf position immediately above (inside) ebL 1 is uL 1, and the positions further up (inside) are labeled acropetally uL 2, uL3, and so on. The leaf length ranged from 2.96 (ebL16) m to 5.37 m (ebL3) (Fig. 12.3b). The leaf length of ebL 2 was shorter than that of ebL3 because the petiole of ebL 2 was elongating and did not reach its final length. The number of leaflets per leaf ranged from 62 (ebL16) to 86 (ebL2). In regard to unexpanded leaves, the leaf blade of uL 2 started to elongate rapidly (Fig. 12.3c) and would reach its final length by the time the position of the leaf becomes ebL2. Although the leaf petiole of ebL 1 could not be measured due to the invisible position at which the lowest leaflet attached, the petiole of ebL 1 would start to elongate rapidly and reach its final length by the leaf position of ebL 3. These results suggested that emergence of a spear leaf (ebL 1) should be attributed to the elongation of the leaf blade and petiole during the rosette stage. After trunk formation, the leaf blade elongated to its final length during the period, from the leaf position of uL 3 to that of ebL 1, and the leaf petiole elongates rapidly at the position of ebL 1 (Nakamura et al. 2015).

### *12.3.2 Development of Leaflets*

The Arecaceae family includes palms with induplicate leaves such as in the date palm and with reduplicate leaves such as in the coconut palm. In leaves with induplicate segmentation, the leaflets are V-shaped in transverse section with the singlefold abaxial; in leaves with reduplicate segmentation, they are Λ-shaped with the single-fold adaxial (Tomlinson 1990). Sago palm has reduplicate leaves (Goto and Nakamura 2004); however, little has been reported on the leaf formation process of sago palm.

Figure 12.4 represents the cross section of the lower part of a spear leaf after trunk formation and unemerged young leaves of the sago palm shown in Fig. 12.3. The midribs of leaflet are on the adaxial side and the edges of leaflet are on the abaxial side (Fig. 12.4a, b). When splitting occurs along the abaxial ribs, leaflets that are Λ-shaped in section form. These suggest that splitting would occur along the abaxial ribs in sago palm. A number of pleats with alternating ridges and furrows are observed in uL2 to uL 4 (Fig. 12.4c, d). The midrib of leaflet might be

**Fig. 12.3** (**a**) A sago palm with no spines 3.3 years after transplantation, (**b**) characteristics of expanded leaves, and (**c**) unexpanded leaves (From Nakamura et al. 2009)

**Fig. 12.4** Cross section of the lower part of a spear leaf of plant after trunk formation (**a**) uL1, (**b**) young leaves from uL2 to uL5, and (**c**–**e**) of the sago palm at rosette stage (shown in Fig. 12.3a)

formed in the ridges on the adaxial side. Among the palms with pinnate compound leaves, Dengler et al. (1982) reported on the morphogenetic process in the early stage of leaflet formation in *Chrysalidocarpus lutescens* (=*Dypsis lutescens*). A similar morphogenetic process is expected to occur in sago palm. Further studies are needed for confirmation.

### *12.3.3 The Number of Unemerged Leaves*

An understanding of the number of unemerged leaves is useful for growth analysis of sago palm. Flach and Schuiling (1989) reported that the number of unemerged leaves was 24, which was the same as the number of green leaves in the crown, in the early stage of trunk formation. Nakamura et al. (2015) reported that the number of unemerged leaves of a tree with 15 emerged leaves 4 years after trunk formation was 18 and that of a tree with 17 emerged leaves 8 years after trunk formation was 19. Nabeya et al. (2015a) found that there was a close relationship between the diameter of the attached part of a spear leaf and the number of unemerged leaves of suckers of proper size for transplantation. This result suggests that the number of unemerged leaves inside a spear leaf increases with an increase of the diameter of the attached part of a spear leaf. The diameter of the attached part of a spear leaf may be an indicator of the unemerged leaves; however, further studies are needed on the details of leaf formation.

### **12.4 Stem**

### *12.4.1 Stem Formation During the Rosette Stage*

The stem of a transplanted sucker creeps in a straight line on the ground. The creeping direction remains the same later when the sucker is transplanted. According to observations of the longitudinal section of stem, morphological characteristics such as nodes are not recognized clearly (Nabeya et al. 2015d). Representing the nodal planes, which were estimated as the positions of attached leaves, the nodal planes coincided with an angle of about 40° to the ground (Nabeya et al. 2015d). In other words, during the rosette stage, sago palm stems are formed by the horizontal line of thin disciform internodes with an angle of about 40° to the ground.

### *12.4.2 Creeping Elongation of Sucker Stems*

It is important to know the creeping elongation rate of the stem and the distance from the transplanted position or the attached position to the mother stem to the trunk stand position in order to manage the density of a trunk stand properly. A few studies have focused on this. According to an approximately 8-year observation of the stem length in the creeping part of transplanted suckers by Nabeya et al. (2015c), the creeping part length increased exponentially from transplantation to around 4 years thereafter, and gradually increased slowly, suggesting that the growth curve was sigmoidal. The length from the transplanted position to the trunk stand position ranged from 1.62 to 2.05 m (avg. 1.81 m) 7.8 years after transplantation (YAT 7.8) (Fig. 12.1). As a result of growth analysis for creeping elongation of the sucker stem, the maximum elongation rate was estimated as 0.38 m per year at YAT 3.8.

Nabeya et al. (2015c) also observed the growth of the derivative suckers such as primary suckers from the main sucker and secondary suckers from the primary suckers, finding that the creeping part length from the attached position to main stem to the trunk stand position was about 1.7 m away in the primary suckers which formed trunks. However, the elongation rate of the primary suckers which were in the rosette stage ranged from 0.11 to 0.14 m per year, and the increasing rate of leaf numbers of them was slower than the main suckers. As the main sucker forms a trunk and elongates vertically, the position of the crown is higher, implying that the amount of sunlight that the derivative suckers receives decreases. The low elongation rate and the low increasing rate of leaf numbers of these suckers could be attributed to the low sunlight due to crown shading of main suckers which formed a trunk. Further studies on the growth of not only main suckers but also derivative suckers are needed to establish the sustainable cultivation of sago palm with high starch productivity.

### **References**

**Open Access** This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

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### **Chapter 13 Morphological and Anatomical Characteristics of Sago Palm Starch**

### **Yoji Nitta**

**Abstract** Amyloplasts, in which starch granules accumulate, are formed near the apical portion of sago palm stems. Amyloplast separation and division occur abundantly and specifically in the apical portion and in the basal stem during the middle and even in the late growth stage. Because of those separations and divisions, amyloplast sizes differ greatly among varieties and stem portions within a plant. The numbers of amyloplasts in the cross-sectional area of the parenchyma tissue also differ among cultivars. Generally, a stem parenchyma cell has 10–30 amyloplasts. Most amyloplasts are egg-like structures with a smooth surface. Still, the sago palm starch grain size is situated in the middle of grain sizes of 54 examined plant species. Furthermore, intercellular spaces are large in sago palm stem tissue, accounting for nearly 40–50% of their total space. This specific feature is a causal factor supporting the starch yield. These results suggest that the separation and division, amyloplast shape, amyloplast size diversity, and large intercellular spaces are specific to sago palm stems. Moreover, intercellular spaces are large in stem tissue, which might be a factor strongly affecting the starch yield.

### **13.1 Introduction**

In higher plants, starch accumulation features are widely diverse among species, cultivars, and varieties, as are storage organs such as seeds, grains, roots, and stems. In the case of sago palm, great amounts of starch are accumulated in parenchyma cells in the stem (trunk). Within the stem, starch accumulates in cell organelles, called amyloplasts, in the center of ground parenchyma.

Many crops produce and accumulate starches. However, starch storage organs differ among crops: (A) grains are used by rice, wheat, corn (maize), barley, and other cereal crops; (B) tubers are used by potato, Jerusalem artichokes, and arrowroot; (C) tuberous root are used by sweet potato, cassava, dahlia, and snake gourd plants; and (D) other organs are used by lotus and banana plants.

Y. Nitta (\*)

The College of Agriculture, Ibaraki University, Ami, Ibaraki, Japan e-mail<EMAIL_ADDRESS>
Regarding starch accumulation in an amyloplast, if starch grains accumulate there, they are called *simple starch grains* such as sago palm stems, potato tubers, and yam tubers. If multiple starch grains accumulate in an amyloplast, the starch accumulation is called *compound starch grains* such as rice grains, taro tubers, and sweet potato tuberous roots.

For cereal crops, accumulation features of stored substances such as starches, proteins, and lipids have been investigated intensively, suggesting that starch accumulation features are widely diverse among species, cultivars, and varieties as well as growing area, culturing methods, and environmental conditions. Starch accumulation features of sago palm stem are also diverse.

As described in this paper, morphological and anatomical characteristics of starch accumulation features in sago palm stem are explained using a specific method and procedures with electron microscopy.

### **13.2 Research Methodology**

Observation using scanning electron microscopy requires specific procedures because plant tissues, cells, and starches in parenchyma cells have an artifact structure during material preparation for observations and require charged viewing during observation. General preparation procedures for observation by scanning electron microscopy include the following: dissection of stem portions of small volumes (5 mm length × 5 mm width × 2 mm thickness) is preferred for materials. They are subjected to rapid freezing using slush nitrogen (−210 °C) followed by vacuum freeze-drying (−60 °C, 10−<sup>3</sup> Pa) (Matsuda 2003). Subsequently, the revealed cross-sections were coated by OsO4 and/or platinum. In our laboratory, we use a scanning electron microscope (JSM6360A; JEOL, Japan). Cell and/or tissue crosssectional areas are also measured using a personal computer with specific software (WinROOF; Mitani Corp., Japan).

This paper presents a summary of observation results obtained using several materials as follows.

(E) Stem. Collected at the Municipal Agriculture Training Center in Burauen, Leyte Province, Philippines, in July 2007.

Furthermore, potato tubers, Chinese yam tubers, wheat grains, edible canna tubers, rice grains, sweet potato tuberous roots, and eddoe tuberous roots were used derived from our laboratory collection.

### **13.3 Morphological and Anatomical Features of Sago Palm Stems and Starch**

### *13.3.1 Internal Structure of Sago Palm Stem*

In sago palm, starch is accumulated in parenchyma cells in the stem.

Monocotyledonous plants, like the sago palm, have no interfascicular cambium for secondary thickening and growth. Sago palm stem thickening depends solely on its primary growth and moreover has great ability and activity for thickening and growth from their apical portion to the base.

The sago palm stem encloses large intercellular spaces (Fig. 13.1) (Nakayama et al. 2007; Warashina et al. 2007). The percentage of intercellular spaces in the cross-sectional area of stem parenchyma is as great as 40–50%. Scanning electron microscope observation revealed that intercellular spaces are formed by surrounding six to eight parenchyma cells in the apical part of the stem (Fig. 13.1). A *honeycomb structure* produced by surrounding parenchyma cells was also observed, indicating the physical strengthening of the stem structure.

**Fig. 13.1** Scanning electron micrographs of parenchyma and intercellular spaces of sago palm stem: (**a**) apical meristem portion, (**b**) middle position of stem, *P* parenchyma, *I* intercellular space, Bar: 10 μm (Source: Nakayama et al. 2007)

### *13.3.2 Starch Accumulation Structure in Sago Palm Stem*

In higher plants, starch granules accumulate in amyloplasts. Jong (1995) measured the long axes of amyloplasts in parenchyma cells of sago palm stem from after the trunk formation stage to the full trunk growth stage and the fruit ripening stage and reported that amyloplasts are longer at later stages of development. According to Ogita et al. (1996), amyloplasts within the stem parenchyma aged 3, 5, 8, and 13 years showed differences with increased age. They found that the major axis of the amyloplast was 5–20 μm in 3-year-old palms, 20–30 μm in 5-year-old palms, and greater than 30 μm in 8-year-old palms or 13-year-old palms. Kawasaki (1999) and Kawakami (1975) reported that when sago palm amyloplasts are compared with simple starch grains (simple starch grain type as described above) in other plants, they are larger than those in wheat (secondary starch granules, 2–8 μm diameter; primary starch granules, 20–40 μm diameter) or yam (about 20 μm diameter) but smaller than those in potato (10–90 μm diameter) or edible canna (40–100 μm diameter) (Table 13.1). In comparison with amyloplasts containing compound starch granules (compound starch grain type as described above), they are larger than those in rice (2.0–8.0 μm diameter), sweet potato (8.0–36.0 μm diameter), or taro (0.13–0.42 μm diameter). Jane et al. (1994) also reported from comparison of 54 crop species that sago palm amyloplasts are regarded as medium-sized among simple starch grain crop species.

**Table 13.1** Characteristics of starches of several crops

Source: Nitta et al (2010)

### *13.3.3 Amyloplast Proliferation*

Starch production of simple starch grain crops depends on the number and size of amyloplasts that contain starch. Proliferation of amyloplasts differs greatly among crops. In sago palm stems, the proliferation feature of amyloplasts is more specific than in other crops.

Nitta (2014) reported amyloplast proliferation of sago palm stems as follows (Fig. 13.2): a plastid, which is a precursor of an amyloplast, is formed near the apical portion. After commencement of starch accumulation, a plastid becomes an amyloplast. Amyloplasts are cell organelles after starch accumulation within a plastid.

Amyloplasts in the early growth stage are mostly oval-shaped or spindle-shaped with a smooth, round surface. Many amyloplasts develop a protuberance in one part of the oval or spindle body at the middle stage of growth. In addition, a part of the oval or spindle has separated or is about to separate in many amyloplasts. The planes of separation are very flat and smooth.

Some amyloplasts separate in more than one place. No protuberance exists on the amyloplast surface after separation or immediately before separation in many cases.

In short, amyloplast proliferation of sago palm stems proceeds in the following manner (Fig. 13.2):

These proliferation features, separation and division, occur in amyloplasts at or after the middle growth stage and in large amyloplasts at the early growth stage. In the protuberance, a stroma is apparently localized inside.

### *13.3.4 Amyloplast Size and Number Among Varieties*

Mizuma et al. (2007) reported that the size and number of amyloplasts vary according to the position within the stem or by variety. Experiments using six sago palm varieties growing on the shores of Lake Sentani near Jayapura, Papua Province, Indonesia, close to the place of origin of sago palms, reveal that the major axis in all varieties is longer in amyloplasts in the middle and lower positions of the stem than in the upper positions. These results demonstrate that separation and division occur frequently in the middle and the lower positions of the stem. The major axis is short at the lower stem in Rondo and Para, suggesting that separation and division occur with high frequency on the basal side of the middle stem. The minor axis is also longer in the middle and lower positions than in the upper position in all varieties.

The numbers of amyloplasts in the cross-sectional area of the parenchyma tissue also differ among cultivars. Our experiments have found the most numerous amyloplasts in Rondo (262.4 mm−<sup>2</sup> ) and the fewest in Para Wiliha (184.4 mm−<sup>2</sup> ).

Starch accumulation features of potato tuber, Chinese yam tubers, wheat grains, and edible canna tubers are those of simple starch grain, while those of rice grains, sweet potato tuberous roots, and eddoe tuberous roots are those of compound starch grain. The starch major axis is longer in simple starch grains than in compound starch grains (Fig. 13.3).

However, considerable differences among varieties were observed in terms of the amyloplast size (Nitta et al. 2005, 2006, 2007). The major axis was longest in Pala Hongleu (38.7 μm) and shortest in Para Wiliha (27.7 μm).

In all varieties, the number of amyloplasts per unit cross-sectional area in the stem parenchyma is larger in the upper position than in the middle or basal position. Rondo and Yepha Hongleu, however, had more numerous amyloplasts in the lower position of the stem than in the middle, suggesting that separation and division occur frequently in these stem positions.

**Fig. 13.3** Starch accumulation and amyloplast structures of several crops: (**a**) sago palm stem parenchyma; (**b**) potato tuber; (**c**) Chinese yam tuber; (**d**) wheat grain; (**e**) sweet potato tuberous root; (**f**) eddoe tuberous root; Bars, 10 μm; *A* amyloplasts. Amyloplasts include starch granules

### *13.3.5 Sucker Structure and Starch Accumulation*

In sago palm-growing areas such as Indonesia and Malaysia, transplanting is conducted using suckers for maintaining and propagating sago stubs. Suckers are formed in the basal portion of the mother stem accompanied by several emerging leaves. When the stem base diameter reaches about 10 cm, the sucker can be detached from the mother stem and transplanted into the field after brief nursery cultivation. Therefore, adequate management based on morphological and physiological characters is needed for rapid growth after transplantation.

In sago palm suckers, the cross-sectional area of parenchyma cells is larger in the lower stem portion. Intercellular spaces are formed even in the apical portion of the stem, followed by their enlargement in the lower stem portion. These features are almost identical to those of the main stem, as described above.

Plastid accumulates starch to become an amyloplast, followed by amyloplast enlargement. Amyloplasts, which are round and smooth, are formed in the apical meristem portion of the stem.

The occurrence of separation and division of amyloplasts is not often observed. Major and minor axes of amyloplasts are smaller in the upper stem portion. Arai et al. (2009) reported that suckers show not only early growth of parenchyma cells and tissues but also more rapid starch accumulation in amyloplasts than in the mother stem (Warashina et al. 2009) at the same distance from the apical meristem portion.

As described above, amyloplasts are formed in the apical meristem portion of sago suckers. They are round and smooth, with few occurrences of separation and division. These features differ from those of the mother stem.

### *13.3.6 Gelatinized Feature of Sago Palm Starch*

One sago palm starch cooking method is heating in water. By heating in water, starches included in the sago palm swell and gelatinize. Gelatinized starch and nongelatinized starch of commercialized sago palm starch after heating to 60 °C in water were assessed using scanning microscopic observation and comparison to starches of other species.

In gelatinized portions of sago palm starch, small holes of several micrometers in diameter are observed. Gelatinized starches are integrated into neighboring tissues. Holes of several micrometers in diameter and a thick skeleton structure are apparently causal factors of stickiness. Small pits (within several micrometers) were observed on the gelatinized starch surface.

Boiled sago palm starch, which is sold in city markets, revealed two distinct portions: a portion showing advanced gelatinization and a portion showing no advancement with remaining starch granules.

Stem materials of the Rondo cultivar are well known to be eaten after boiling in water in Indonesia. Scanning electron microscopic observations reveal that structures of vascular bundles, cells, and other tissues were not changed after boiling. However, boiling has advanced gelatinization not only within cells but also at the tissue level, including surrounding cells.

### **References**

**Open Access** This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

### **Part V Growth Environment**

### **Chapter 14 Soil Environment in Sago Palm Forest**

**Masanori Okazaki and Yuka Sasaki**

**Abstract** Soils (acid sulfate soils, peat soils, gley soils, and others) distributed under sago forest and their productivity of sago palm are described in this chapter. Sago palm in tropical lowland areas is growing with the formation of the communities behind the mangrove forest. The main sources of water for sago palm are rivers, which are present in the eutrophic environment and more or less affected by sea tides. Sago palm equipped with the mechanism to eliminate salt effect or regulate salt uptake in several ways can grow in brackish water. Acid sulfate soils are derived from sulfate ion (SO4 <sup>2</sup>−) in seawater. Sulfate ion is reduced to form sulfide compounds by sulfate-reducing bacteria in soils (potential acid sulfate soils). Sulfide compounds are oxidized to sulfate ion and hydrogen ion is produced by sulfur- and iron-oxidizing bacteria in soils (actual acid sulfate soils). The sago starch yield is observed to be extremely high near the coast and lower in the inland places (soil pH 3.3–3.8). The tropical woody thick peat soils called Histosols in the tropical rainforest climate of Southeast Asian islands are formed to transport small amount of sediments by the shorter rivers compared to large rivers of continents. The constituent components in water flowing into tropical peat soils ensure the normal growth of sago palm. In Sarawak no effect of nitrogen (N) application on leaf production of sago palm was found, which was explained by the findings of endophytes' activities on the nitrogen fixation. The sago palm growth in Inceptisols of the Philippines and Indonesia at the different stages was larger than those in Histosols of Malaysia from the long-term growth study.

M. Okazaki (\*)

Japan Soil Research Institute Inc., Nishitokyo, Tokyo, Japan e-mail<EMAIL_ADDRESS>
Y. Sasaki Faculty of Agriculture, Yamagata University, Tsuruoka, Yamagata, Japan

### **14.1 Natural Habitat of Sago Palm in Tropical Lowland Areas**

Natural lowland forest in tropical areas consists of mangrove, tropical lowland, and tropical peatland forests, in that order moving inland from the sea (Okazaki et al. 2008) (Fig. 14.1). Although distributed in both tropical and subtropical lowland areas affected by seawater, the dominant distribution of mangrove forest is present in tropical brackish water areas. Brackish water is defined as a mixture of sea- and freshwater with a salt concentration of 0.2–30 parts per thousand (‰), equivalent to 1/100–1 of the salt concentration of seawater, because seawater generally contains 33–34‰. Nipa and sago palm are present behind mangrove forest and form a large plant community. Both tropical lowland forest and tropical peatland forest are found in brackish water areas, each with a different freshwater source. Tropical lowland plants grow under relatively eutrophic nutrient conditions, while tropical peatland plants are under poor nutrient conditions and affected by rainfall and flowing groundwater with high reduction and oxidation (redox) potential (Table 14.1).

Sago palm (*Metroxylon sagu* Rottb.) is part of the formation of vegetation communities behind the mangrove forest (Yamada 1986) (Table 14.1). In the very poorly drained to swampy conditions of Papua New Guinea, sago palms and pandans (*Pandanus*) are found in the understory (Bleeker 1983). The main source of water for sago palm is the rivers, which are present in the eutrophic environment and more or less affected by sea tides (Tie and Lim 1977).

**Fig. 14.1** Distribution of tropical lowland forest along the sea (Okazaki et al. 2008, partly modified)

**Table 14.1** Typical tropical plant communities (Yamada 1986)

Halophytic plants equipped with mechanisms to eliminate salt effect or regulate salt uptake in several ways can grow in brackish water. Flach et al. (1977) found that sago palm was not inhibited in a Hoagland solution of about 6–7 millisiemens (mS) per cm electrical conductivity, which corresponds to 1/7–1/8 of electrical conductivity of seawater. However, the growth rate of sago palm slowed when this range of electrical conductivity was exceeded. Many terrestrial plants suffer from a salt concentration of 0.1%, and significant growth suppression is found when it exceeds 0.3% (around 60 mmol L−<sup>1</sup> ) (Matoh 2002). Salt stress is divided into two types: the inhibition of water absorption due to osmotic pressure generated by salt (osmotic stress) and the excess damage caused by the specific physiological effects of the salt-constituting ions (ionic stress). Generally ionic stress is regarded as the primary factor of salinity stress. As sago palm is highly tolerant of salinity stress, it is likely to be equipped with several kinds of mechanisms. By the treatment of 0–0.2% sodium chloride solution, sago palm absorbed sodium ions from the root and translocated them to the petiole and the leaflets. However, sago palm seedlings retained sodium ions in the roots and transferred them to the lower leaves gradually (Ehara et al. 2006). Yoneta et al. (2004, 2006) determined that sago palm seedlings grew best at a salt concentration of around 10 mmol L−<sup>1</sup> (1/60 of sea salt concentration), while sago palm growth was inhibited in water or in a salt concentration range of 50–200 mmol L−<sup>1</sup> (Fig. 14.2). Ehara et al. (2008) cultured *Metroxylon sagu* Rottb. and *M. vitiense* for 1 month hydroponically; thereafter a 2% sodium chloride solution was used for the culture for another month. Results showed that the transpiration rate of all sago palms declined with the treatments and that the potassium content in sago palm increased with increasing sodium content in the petiole. Yoneta et al. (2006) deduced that sago palm primarily maintained a high osmotic pressure

**Fig. 14.2** Changes in the height of sago palms under different NaCl concentrations (Yoneta et al. 2006)

**Table 14.2** Soils related to sago palm growing areas (common name, US Soil Taxonomy)

in the cytoplasm using potassium ions as the osmotic pressure regulator (compatible solute). They concluded that small amounts of other compatible solutes such as proline and glycine betaine were produced. In addition, Ehara et al. (2003, 2006) showed that sago palm roots excluded sodium ions using the barriers to inhibit sodium ion absorption.

### **14.2 Soils Distributed Under Sago Palm Forest**

In this chapter, soil names (common and US Soil Taxonomy names) distributed beneath sago palm forests are shown in Table 14.2.

### **14.3 Acid Sulfate Soils (Typic Sulfaquents, Sulfic Hydraquents, Sulfic Tropaquents, Typic Sulfihemists, etc.)**

The pedogenic process of acid sulfate soils requires a source of sulfate (SO4 <sup>2</sup>−: 2650 mg/L) derived from seawater and brackish water to supply organic matter as an energy source for heterotrophic bacteria (*Desulfovibrio* and *Desulfotomaculum*), resulting in the formation of S2− and S0 (Kyuma 1986). The reaction of Fe2+ and S2<sup>−</sup> gives ferrous sulfide (FeS). Ferrous sulfide reacts S0 to form FeS2 (pyrite) (Figs. 14.3 and 14.4). Fe2+ and S2− in FeS2 are oxidized to Fe3+ mediated by *Thiobacillus ferrooxidans* and *Ferrobacillus ferrooxidans* and SO4 <sup>2</sup>− mediated by thiobacilli groups (Fig. 14.5), respectively. Jarosite (KFe3(SO4)2(OH)6 and goethite (α-FeOOH) are produced which are pale yellow (2.5 Y 6/8–2.5 Y 8/8) and yellow brown (Fig. 14.6). Clayey yellow brown sediments in acid sulfate soils are called *cat clay*, which derives from the Dutch term *katteklei*.

In the 1840s, sago palm cultivated in Sarawak was grown quite successfully in some parts of the island (Borneo), and the raw sago exported in large quantities from the west coast to Singapore (Fukui 1980; cited from Low 1848). *Metroxylon sagu* is still the main food of several Papua groups in New Guinea; the inhabitants of most of the islands in the Moluccas; the southeast arm of Sulawesi; the Banggai and Sula archipelagoes east of Sulawesi; the Mentawai Islands west of Sumatra; the Melanau people in Sarawak; the east coast of Sumatra (Bengkalis); in the Riau, Karimun, and Lingga archipelagoes; and in some coastal regions in west Kalimantan (Avé 1977). The proper growing areas for sago palm are *tana nabo* (peat soils con-

**Fig. 14.3** Pyrite in acid sulfate soils

**Fig. 14.4** X-ray diffraction pattern of HF-treated acid sulfate soil

**Fig. 14.5** Thiobacillus in acid sulfate soils

taining alluvial sand and clay) and *tana pala* on the interfluves produced by rivers in their meandering in Sarawak (Morris 1953). The peat soils (*tana guun*) away from the river, however, give rise to fast growth of sago palm, but they are poor in sago starch content. The sago palm-growing areas, however, are often composed of alluvial soils and peat soils (Sato et al. 1979). Flach (1983) revealed that sago palm grew best in mineral soils which should be high in organic matter as opposed to peat soils and that clay soils were usually found in the natural habitat of sago palm.

The soils under sago forest in South Sulawesi, Indonesia, (Tables 14.3 and 14.4) are located in transition areas between the natural river bank and black marsh (Takaya 1983; Okazaki 1995). Soils that are already strongly acidic are called *actual acid sulfate soils* (Table 14.3), and those which become acidic after oxidation are called *potential acid sulfate soils* (Table 14.4).

**Fig. 14.6** Jarosite and goethite in acid sulfate soils

**Table 14.3** Soil profile in Desa Takkalala, Kabupaten Luwu, South Sulawesi, Indonesia (Takaya 1983, partly modified)

Profile A (Center of sago forest)

3–0 cm, L, litter horizon, sago and other leaves

0–82 cm, B, light gray color in matrix, coarse texture, bright brown (7.5 YR 5/6 to 5/8) to brown (7.5 YR 4/3 to 4/6) of tube type mottles with diffusing outside, 2–3 cm structure in diameter, present gley mottles, many fresh and old sago roots (5–7 mm in diameter) in the structure, yellow (fresh roots) and black (old roots) color roots surrounded by blue gray (reduced) color parts

**Table 14.4** Soil profile in Tobimeita, Kendari, South Sulawesi, Indonesia (Okazaki 1995)

Profile B (Sago forest, potential acid sulfate soil)

0–7 cm, A, surface horizon, very yellowish brown (10 YR 5/5), moist, coarse sand, structureless, few medium and fine weed roots, pH 7.8, EC 0.30 mS/cm, clear smooth boundary to

7–35 cm, B1, grayish olive (5Y 5/2), moist, coarse sand, structureless, few organic debris with original shape and decomposed shape, pH 6.5, EC 0.32 mS/cm, clear smooth boundary to

35–70 cm, B2, brownish black (2.5 YR 3/2) in matrix and black (2.5 Y 2/1), wet, silty clay, structureless, common medium and fine sago roots, very sticky, plastic, pH 6.8, EC 0.32 mS/cm, gradual wavy boundary to

70– cm, dark grayish yellow (2.5 YR 5/2), wet, silty clay, structureless, sticky, pH 6.7, EC 0.35 mS/cm

Jalil and Bahari (1991) compared the starch yield of sago palm growing in plantations 0.5, 0.7, and 3.0 km from the seashore (soil pH: 3.3–3.8 in acid sulfate soils) and found that the starch yield was extremely high near the coast and lower in the inland plantations. In Thailand, Nozaki et al. (2004) compared the sago starch content and starch synthetic enzyme activity of sago palms growing in acid sulfate soils and Oxisols and found that the sago growth in acid sulfate soils was lower than that in Oxisols.

### **14.4 Peat Soils (Histosols)**

In continental Southeast Asia under the tropical monsoon climate, rivers have complicated systems, while Southeast Asian islands under the tropical rainforest climate have shorter rivers than on the continents, which transport a small amount of sediments, resulting in the formation of peat soils called Histosols (Fibrists, Hemists, and Saprists) (Fig. 14.7). Trees, shrubs, and grasses that love water can thrive in the areas of high water table and tidal action. Dead plants are broken down usually by decomposers. However, the decomposition processes are inhibited in the areas of high groundwater. Plant residues accumulate to produce peat soils (Histosols), in which plant biomass production exceeds plant decomposition, regardless of temperature (Fig. 14.7).

Histosols are formed in the tropics in areas with high temperature and vigorous woody plant materials and are called *woody peats* (Okazaki 1998). Tropical peat soil is known to form a dome-shaped surface at the final stage of its development (Scott 1985) (Fig. 14.8). Tropical peat soils derived from woody materials in Southeast Asia exhibit strong to weak acidity and lack nutrient elements (Tie and Lim 1991; Yamaguchi et al. 1994). The constituent components in water flowing into tropical peat soils ensure the normal growth of sago palm (Yamaguchi et al. 1998). Sato et al. (1979) reported that the thicker the peat deposit in soil, the slower the sago palm grows and that the sago palm grew better in soil with a thinner peat layer and an underlying argillaceous deposit. In Sarawak 62% of sago palms are grown on Histosols, those with more than 150 cm of surface peats (Tie and Lim 1991). Kueh (1979, 1980, 1981, 1982, 1983) performed a cultivation study of sago palm in undrained tropical peat soils at Stapok in Sarawak and found a depression or no effect of nitrogen (ammonium sulfate) application on leaf production and no effect by P2O5 and K2O, as their results, since 1976. Jaman (1983) found that NPK fertilizer application had no significant positive effect on the rate of leaf production of sago palm in the first year at Sungai Talau Peat Research Station. Jaman (1983, 1984, 1985) carried out experiments of fertilizer application, pruning, weeding,

**Fig. 14.7** Soil profile of tropical peat in Sarawak

**Fig. 14.8** Interrelations between landform units in tropical peat swamps wedged between 2 rivers (Scott (1985), cited from Anderson (1961))

seed germination, spacing, and intercropping related to girth, trunk height, and leaf production and reported that none of the NPK fertilizer application, pruning, weeding, seed germination, spacing, and intercropping had any significant positive effect on the annual leaf production rate of sago palms. Although in the 11th year of growth, trunk height in peat soil under minimal drainage at Stapok Station seemed to be increased by N application (Kueh 1987), there was no significant effect of N application on trunk height in the 13th year of growth (Kueh 1989, 1990, 1995). Kakuda et al. (2000) compared the nitrogen supply in peat and mineral soils. The amount of ammonium nitrogen released from peat soils through mineralization on the 50th day of incubation (100 days in case of transform at 25 °C) was approximately 5.8 mg/kg in Tebing Tinggi, Indonesia, and 4.7 mg/kg in Mukah, Sarawak. It is a property of peat soils that mineralization and nitrogen supply occur more readily as compared with mineral soils. The application of seven times the usual amount of N, P, K, Ca, Mg, Cu, Zn, Fe, and B provided a significant difference of petiole and sucker dry weight (Kakuda et al. 2005). However, no difference was found in other growth factors of sago palm.

The lack of any effect of nitrogen (N) application on sago palm growth is explained by the findings of the endophytes' activities on the N fixation (Shrestha et al. 2006, 2007). When sago palm easily becomes able to absorb N from soils, it does not require the N support by the endophytes. Accordingly it is concluded that the endophytes play an important role in sago palm growth without N application.

Beginning in 1986, Jaman and Jong (1986), Jong and Jaman (1987), Jong (1989, 1990), and Shoon et al. (1995) performed sago spacing (4.5, 7.5, 10.5, and 13.5 m) trials in peat soils in Sarawak and concluded that sago palm should be cultivated in a rectangular pattern of 12 × 8 m to facilitate maintenance work and farm management and suggested around 100 points per hectare. Traditional sago palm cultivation is carried out under minimal management, little sucker control, and no fertilization.

Groundwater level and subsidence related to drainage inhibit sago palm growth and yield of starch. Takaya (1983) and Shimoda and Power (1990) described that sago starch yield declined remarkably or even to zero in permanently submerged land. Flach et al. (1977) found in a sago seedling culture study that the rate of leaf emergence slowed under waterlogged conditions. Hashimoto et al. (2006) also reported that both the number of leaves and the diameter at breast height of sago palms growing in tropical peat soils with an average water table of 57–68 cm were smaller than those in the areas with a lower water table. Kakuda et al. (2015) revealed that sago palms grew better at 50 cm than at 90 cm of groundwater level. The groundwater level around the sago palm root zone is important for growth.

Sugawara (1979) proposed a 10,000 ha sago plantation on areas of tropical peat soils, which strongly required land reclamation and drainage for common tropical crop cultivation and its potential economic effect on Southeast Asian countries. Studies of the relationship between sago (*Metroxylon sagu* and *M. rumphii*) starch quality and soil types (shallow peat soils and mineral soils) in Sarawak were started by Lim and Loi (1987). However, thus far no results have been reported.

### **14.5 Other Entisols and Inceptisols**

Soils eroded by rivers form sediments at the seashore at various rates. The soils along the Sepik River of Papua New Guinea are heavy clays high in organic matter and only flooded seasonally by the Sepik (Holmes and Newcombe 1980). Periodic flooding with water high in mineral elements should provide all of the nutrients required for optimum sago palm growth. Furthermore, Shimoda and Power (1990) reported that the soils of swampy areas in the Sepik River consisted of Hydraquents, Fluvaquents, and in part Histosols, which are poorly drained soils. Shimoda (2000) found the peat horizon at about 1 m depth in a Hydraquent profile. The formation of peat horizons and alluvial materials sedimentation has produced the sago-growing areas in the islands of Southeast Asia.

In Panay, Leyte, Cebu, and Mindanao, Philippines, the habitats of sago palm are predominantly located in Entisols and Inceptisols with periodic flooding and continuous water flow, from 0 to 700 m above sea level (Okazaki and Toyota 2003, 2004). The sago palms in Entisols and Inceptisols grow relatively well, compared to their growth on Histosols mainly utilized for leaf roofing materials in the Philippines, although local people know well how to extract starch in the mature sago palms.

### **14.6 Comparison of Sago Palm Growth Between on Inceptisols and Histosols**

At the same growing stage, a comparison of sago palm has shown that the starch yield per trunk of the sago palm planted in deep peat soils is only 23 % of those planted in mineral soils (Jong and Flach 1995). Okazaki (2012) reported in a longterm growth study that the trunk weights of sago palm growing in Inceptisols of the Philippines and Indonesia at the different stages were larger than those in Histosols

**Fig. 14.9** Difference on biomass (above-ground) of sago palm growing in Inceptisols and Histosols (Okazaki 2012)

of Malaysia (Fig. 14.9). It is concluded that the sago palm growth and starch yield depend on the physicochemical soil characteristics.

### **References**

**Open Access** This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

### **Chapter 15 Microbial Interactions and Activities Affecting Sago Palm Growth**

#### **Koki Toyota**

**Abstract** Microbes are ubiquitous soil inhabitants. Both aboveground and belowground parts of plants are associated with diverse and abundant microbes. Such microbes have positive and negative impacts on the plant productivity. Biological nitrogen fixation (BNF) is such a beneficial interaction. To reveal BNF by freeliving bacteria in sago palm, different parts (root, rachis, petiole, leaflet, bark, pith, and extracted starch) were collected in the Philippines, and their nitrogen-fixing ability was measured. Almost all the samples showed positive nitrogen fixation. Then, nitrogen-fixing bacteria (NFB) were isolated, belonging to different genera, such as *Klebsiella* sp., *Pantoea* sp., *Burkholderia* sp., *Stenotrophomonas* sp., and *Bacillus* sp. All the isolates preferred simple carbon compounds, like glucose, sucrose, and mannitol, as their substrates for nitrogen fixation, while they showed very low activity in starch, pectin, and hemicellulose media. When NFB were cocultured in such a medium with the polymer-degrading bacteria, nitrogen-fixing ability was markedly increased. Stimulatory effects were observed in Rennie medium by co-inoculation of NFB and indigenous bacterial consortia isolated from sago palm samples. These results indicate that complex microbial interactions may increase in situ nitrogen fixation and contribute to nitrogen nutrition in sago palm. This chapter also introduces characteristics of nitrogen-fixing bacteria and amounts of BNF in palm trees in recent studies.

### **15.1 Microbial Activities Relating to Plant Growth**

Microbes exist everywhere, especially in soil. A classic report in Russia revealed that bacteria are a ubiquitous soil inhabitant, and total bacterial numbers are stable across quite diverse soil environments, from dry and desert steppe through meadow steppe, from forest meadow to taiga, and from 1200 to 3600 m above sea level (Mishustin and Mirsoeva 1968). By contrast, they found that specific groups of bacteria favor certain habitats and show large fluctuations depending on time and

K. Toyota (\*)

Tokyo University of Agriculture and Technology, Koganei, Tokyo, Japan e-mail<EMAIL_ADDRESS>
location. For example, spore-forming bacteria, enumerated as heat-tolerant ones, showed large fluctuations in their numbers, ranging from 0.01 to 1.2 × 106 g−<sup>1</sup> soil (more than 100 times difference) depending on the sampling sites, but the differences in total bacterial numbers were only less than five times. Recent studies demonstrate that soil contains as many as 1010–1011 bacteria, 6000–50,000 bacterial species, and up to 200 m of fungal hyphae per 1 g and the soil microbes play key roles in ecosystems (van der Heijden et al. 2008).

In addition to soil, plants harbor a diverse and an abundant microbial community and support their activities as the key primary producers in most terrestrial ecosystems. In particular, the rhizosphere, defined as the soil environment influenced by the presence and activities of plant roots, has a huge impact on soil microbes. Plant roots release organic matter called *rhizodeposition* or root exudate, and the amount of rhizodeposition represents ca. 11% of carbon fixed by the plant and 27% of carbon allocated to roots (Dennis et al. 2010). Rhizodeposition supports the microbial activities in the rhizosphere. A wide range of organisms, i.e., different kinds of bacteria, fungi, protozoa, and nematodes, show higher populations in the rhizosphere than in the non-rhizosphere, which is not affected by plant roots. The rhizosphere consists of endorhizosphere (root tissue area), rhizoplane (root surface), and exorhizosphere (rhizosphere soil: soil directly surrounding the root). According to a report summarizing the results of 22 different plants, the numbers of aerobic bacteria were on average 9.9 times (2.6–24.2) higher in rhizosphere soil than in non-rhizosphere soil (Lochhead and Rouatt 1955), and microbial densities are markedly higher in the rhizoplane than in the endorhizosphere. An example showed that the numbers of total bacteria, Gram-negative bacteria, and fungi were 100–1000 times higher in the rhizoplane than in the endorhizosphere (Fig. 15.1). Rhizosphere soil and the rhizoplane are microbial hot spots, and many microbes colonize even the endorhizosphere.

In addition to belowground, the aboveground parts of plants also support a variety of bacteria, yeasts, and fungi. According to Lindow and Brandl (2003), bacteria are by far the most numerous colonists of leaves, ranging from 106 to 107 cells cm−<sup>2</sup> (up to 108 cells g−<sup>1</sup> ). The aerial habitat colonized by these microbes is termed the *phyllosphere*, and the inhabitants are called *epiphytes*. The number of epiphytes is affected by surrounding environments. For example, Enya et al. (2007) compared the number of leaf-associated bacteria between field-grown and greenhouse-grown tomato leaves and found that the former harbored 100 times higher densities and the population densities increased with age. Since sago palm grows under field conditions, its leaves and stems are colonized by many microbes.

Microbes affect plant productivity through different mechanisms. First, a typical one is direct effects on plants via plant-associated organisms that form mutualistic or pathogenic relationships with plants. Another is indirect effects via the action of free-living microbes that alter rates of nutrient supply and the partitioning of resources (van der Heijden et al. 2008). Plant productivity is enhanced by different microbial actions, while there are a number of microbial threats to crop production (Table 15.1).

Nitrogen-fixing bacteria contribute to plant productivity to the largest extent, as described below. Arbuscular mycorrhizal (AM) fungi enhance plant productivity, especially in grasslands (van der Heijden et al. 1998). These two symbiotic micro-

**Fig. 15.1** The number of microorganisms in the rhizoplane and endorhizosphere of radish grown in soil. *Solid lines*, rhizoplane; *dotted line*, endorhizosphere. All: total culturable bacteria, *G*(−) Gram-negative bacteria, *F* fungi (Toyota et al. unpublished data)

**Table 15.1** Influence of soil microbes on various ecosystem processes (From van der Heijden et al. 2008)

organisms have the greatest impact on plant productivity, but such symbiotic interactions have not been reported in sago palm.

Nutrient supply is an important function of soil microbes. Usually, plants do not use organic forms of N, the dominant form in soil, but use inorganic N, which is mineralized by the actions of soil microbes and animals. Even in agricultural crops

**Fig. 15.2** Origin of N uptake by crops (Drawn from Fujiwara et al. 1996, paddy rice; Brady and Weil 2008, maize; Kato 2004, tomato)

where fertilization is always done, crops absorb more N from the soil organic matter fraction than from applied fertilizer (Fig. 15.2). Since sago palm is often cultivated under non-fertilized conditions, the most important mechanism for its N acquisition is the mineralization of soil organic matter by soil microbes and animals. Indeed, a pot experiment conducted in a glasshouse showed that sago palm growth evaluated by its plant height did not appear to be affected by urea fertilization (Lina et al. 2010), suggesting the importance of the nutrient-supplying capacity of soil.

Direct yield losses caused by pathogens, insects, and weeds are estimated to range from 20 to 40% of global agricultural productivity (Savary et al. 2012). In the natural environment, there are many airborne and soilborne plant pathogens, including fungi, bacteria, viruses, and nematodes. On the other hand, many studies have reported biological control of plant pathogens by epiphytes and rhizosphere microbes.

In sago palm, infestation with the bagworm larvae (*Pteroma pendula*) was found in the Philippines, but its damage to plant productivity was not estimated (Okazaki et al. 2012). As far as the author knows, there is no study reporting damage to sago palm caused by pathogens.

### **15.2 Importance of Biological N Fixation**

Biologically fixed N is a free and renewable resource that plays a key role in sustainable agriculture. Biological N fixation (BNF) is seen to a varying degree in the soil environment including various parts of plants grown in soil. The potential for N fixation exists in any environment capable of supporting the growth of N-fixing bacteria (NFB). The global terrestrial amount of BNF is estimated between 100 and 290 million mt per year (Cleveland et al. 1999), 40–48 million mt per year of which is fixed by agricultural crops in fields (Jensen and Nielsen 2003), corresponding to nearly one-half of global fertilizer usage. Symbiotic BNF in leguminous plants is famous, and N-fixing bacterial symbionts of legumes can contribute up to 20% of all plant N that is annually acquired by vegetation (Cleveland et al. 1999), and its amount reaches as high as 300 kg N/ha/crop. In addition to symbiotic relations, BNF through the activities of free-living N fixers is often seen in non-leguminous plants, e.g., sugarcane (Urquiaga et al. 1992), rice (Shrestha and Ladha 1996), and sago palm (Shrestha et al. 2006). Free-living N-fixing bacteria, which are ubiquitous in terrestrial ecosystems, can also contribute significantly to the N budget of some systems. Cleveland et al. (1999) reported free-living N-fixing bacteria fix relatively small amounts of N (<3 kg N/ha/year), but there are studies reporting larger contributions, such as 3.3–7.8 kg N/ha/year in tropical forest ecosystems (Reed et al. 2011) and 150 kg N/ha/crop in sugarcane (Dobereiner 1997). In oil palm plantations, legume covers are sometimes used under tree crops for the purpose of weed suppression, soil erosion control, and biological control of insect pests (Agamuthu and Broughton 1985). In addition to these, symbiotic BNF is expected; a report found 0.3–34.2 kg N/ha fixed by legume covers (Pipai 2014).

### **15.3 Taxonomy of N-Fixing Bacteria in Palm Trees**

Many free-living N-fixing bacteria have been reported in different crops (Table 15.2). In sago palm, Shrestha et al. (2006) reported that different genera of N-fixing bacteria, such as *Klebsiella pneumoniae*, *K. oxytoca*, *Pantoea agglomerans*, *Enterobacter cloacae*, *Burkholderia* sp., *Stenotrophomonas maltophilia*, and *Bacillus megaterium*, were isolated from the root, rachis, petiole, leaflet, bark, and pith collected from sago palms in the Philippines. *Enterobacter* sp., *Klebsiella* sp., and *Pantoea* sp. were isolated from extracted starch (Shrestha et al. 2007). Shipton et al. (2010) also focused on starch extracted from sago palm trees and isolated *Enterobacter oryzae*, *Klebsiella oxytoca*, and *Cronobacter* (former *Enterobacter*) *turicensis* as N fixers. They also isolated *Pectobacterium* (former *Erwinia*) *cypripedii* from the rhizosphere of sago palm. Few studies have been done on N-fixing bacteria colonizing palm trees. Except for the studies by Shrestha et al. (2006) and Shipton et al. (2010), Reis et al. (2000) reported that oil palm was colonized by *Azospirillum brasilense*, *A. amazonense*, and *Herbaspirillum seropedicae*, and Tang et al. (2010) reported that *A. amazonense* was isolated from the root of sago palm and that *Burkholderia vietnamiensis* and *B. kururiensis* from the root of nipa palm. The genus *Azospirillum* is a Gram-negative free-living N-fixing rhizosphere bacterium, and *A. amazonense* was first isolated from roots and rhizosphere soil of Gramineae, in the Amazon region, Brazil (Steenhoudt and Vanderleyden 2000). *Burkholderia vietnamiensis* was the only known N-fixing species of this bacterial genus and was first isolated from the rhizospheres of rice, maize, and coffee plants (Santos et al. 2001). Since then, several species have been isolated from the endophytic environment of a wide range of taxonomically unrelated plants such as maize, sorghum, sugarcane,

**Table 15.2** Lists of free-living N-fixing bacteria isolated from different plants

pineapple, and coffee, and currently nine diazotrophic plant-associated *Burkholderia*, including *B. kururiensis*, have been validly described (Wong-Villarreal and Caballero-Mellado 2010). These studies conclude that palm trees harbor N fixers such as facultative anaerobic enteric bacteria, *Burkholderia* and *Azospirillum*, which have been also isolated from major crops, such as rice and maize.

### **15.4 Enhancement of N-Fixing Ability by Microbial Interactions**

BNF requires many factors; the most important element among them is a carbon substrate. In symbiotic BNF, abundant substrate is provided through photosynthesis by the host plant, while in free-living BNF, a crucial issue is how to obtain enough substrate for the energy source. For that reason, many free-living N-fixing bacteria are associated with plants. In general, NFB utilizes exclusively simple carbon sources like glucose and sucrose (Haahtela et al. 1983). In contrast, the major carbohydrates in plants are complex carbon sources like cellulose, hemicellulose, and pectin (Lack and Evans 2001). Thus the effects of microbial interactions between NFB and indigenous bacteria, both of which were isolated from sago palm, on BNF were investigated. All NFB isolated from sago palm preferred simple sugars, like glucose, sucrose, and lactate, as their substrate for N fixation and showed extremely low levels of N-fixing activity in starch, hemicellulose, and pectin-containing media (Fig. 15.3) (Shrestha et al. 2007). N-fixing activity by NFB was markedly enhanced by the consortium of starch-degrading *Bacillus* sp. strain B1 in a starch medium, although the NFB showed negligible N-fixing activity when inoculated singly (Fig. 15.4). The consortium of hemicellulose-degrading *Agrobacterium* sp. strain

**Fig. 15.3** Nitrogen-fixing activity of nitrogen-fixing bacteria in different carbon substrates. *Glu* glucose, *Suc* sucrose, *Lac* lactate, *Pec* pectin (Shrestha et al. 2007)

**Fig. 15.4** Effect of co-inoculation of nitrogen-fixing bacteria (S1, S2, R1, and R2) and polymerdegrading bacteria on the nitrogen-fixing activity in polymer media (Shrestha et al. 2007)

**Fig. 15.5** Effects of co-inoculation of randomly isolated strains (each group consisted of ten strains) on nitrogen-fixing ability of nitrogen-fixing bacteria (R1 and R2) (Shrestha et al. 2007)

HMC1 or *Flexibacter* sp. strain HMC2 and NFB also showed enhanced N-fixing activity in a hemicellulose medium. Such stimulation was not observed in a pectin medium. These results suggest that N-fixing bacteria may actively fix N in collaboration with degraders of starch and hemicellulose, the major carbohydrates in sago palm plant bodies.

The second important parameter in BNF is an oxygen level which affects nitrogenase activity directly (Robson and Postgate 1980). Coculture of NFB and indigenous bacteria, isolated from sago palm using nutrient agar medium, in a nitrogen-free Rennie medium containing simple organic compounds showed significantly higher N-fixing activity than single inoculations of NFB did in almost all combinations (Fig. 15.5), suggesting that co-inoculated bacteria consumed O2 and made conditions with deficient O2. Indeed, we confirmed that a reduced oxygen status itself enhanced the N-fixing activity of NFB (Fig. 15.6) (Shrestha et al. 2007).

**Fig. 15.6** Effect of ambient (*white bar*) and reduced O2 (*gray bar*) conditions on the nitrogenfixing activity of selected nitrogen fixers (R1, R2, R3, and R4) (Shrestha et al. 2007)

These results may indicate that beneficial microbial interactions occur in sago palm to enhance N-fixing activity through collaborative utilizations of starch, hemicellulose, and their degradation products.

### **15.5 Estimate of Amounts of N Fixation in Palms**

Shrestha et al. (2006, 2007) quantified N-fixing activity in different parts of sago palm, such as stem, leaf, root, bark, and starch, and isolated a wide range of N-fixing bacteria. Although the estimation of fixed N based on the acetylene-reducing activity contains some uncertainties, the amount of fixed N in a mature sago palm stand was estimated at 210 kg N/ha/y from calculation based on N-fixing activity in root (221 nM C2H4/g/day), pith (213 nM C2H4/g/day), and leaf sheath (35.4 nM C2H4/g/ day) and their mean weights per palm (68, 721, and 97 kg in root, pith, and leaf sheath, respectively) with a sago palm density in a mature forest of 923 sago palms/ ha (Toyota 2015).

Yonebayashi et al. (2014) estimated the amount of N fixation in sago palm using a tracer experiment. They measured δ15N values of the youngest leaves of sago palms at different stages of growth and found that δ15N values were lower with age, indicating higher N fixation with maturing. The contribution of biologically fixed N to total N of sago palm leaves was less than 10% at the beginning of growth stage (3 years), but it increased with age and reached more than 90% at the later stage (13 years).

Amounts of N fixation have been estimated in other palms. De Carvalho et al. (2008) reported that 13–76% of total N in oil palm depended on biological N fixation in a 1-year growth experiment using N poor quartz sand and subsoil. Zakry et al. (2012) found that the contribution of biological N fixation to total N uptake by oil palm was different depending on the plant parts in oil palm (75% in leaflet, 13% in stem, and 13% in root) and was 63% on the whole plant basis. These results reveal that BNF functions as a biofertilizer and is essential in establishing sustainable crop production.

### **References**

**Open Access** This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

### **Part VI Starch Production and Utilization**

### **Chapter 16 Sago Starch: Transformation of Extraction and Consumption Processes in Traditional Indonesian Societies**

**Yoshihiko Nishimura**

**Abstract** New Guinea Island (NGI) is the origin of sago palm. Sago became a food plant not only in NGI but was also dispersed to Asian areas for use as a staple food. In the current study, the transformation of extraction technology and the trends in sago consumption were surveyed in the area of sago origin and the other areas subsequently adopted sago palm in Indonesia. The original starch extraction method was to pulverize the sago pith with an ax and wash the pieces of pith by hand, which was practiced in NGI. Then this technology of starch extraction was transferred to western Indonesia through the process described below.

*Pith pulverization*: Original form of pith crushing by ax (chopping with an ax while sitting and a long ax while standing) transferred to west part of Indonesia and Malaysia, followed by further development in grater forms and adaptation to rasper machine use.

*Washing pieces of crushed pith*: Original form of washing by hand was transferred to the west for further modification of crushing the pith by foot with highpressure water (pumping and gravity) form. This form of washing by water flow is a transformation from a horizontal to a vertical direction.

Sago starch is used for various foods from *papeda* (dough type with soup) as a staple food to confectionery products (*lempeng*, baked crackers, cookies, or jellies), noodles, and dry powder (a substitute for other starches).

An important aspect of sago production system depends on farmers' needs, whether they sell it or utilize it themselves. The next important issue is to increase production for the commercial market. In this step, group production system is adapted in the process. This group work is performed by farmers which is the target for specialized business. In addition, mechanization has been introduced, like using a rasper for grating and a pump for washing the pith. These transformations indicate how to develop an efficient economic output. Sago is changing from the concept of staple food to other starch food uses and starch goods use, as the social economy and cash-based economy are developed in the rural Indonesian society.

Y. Nishimura (\*)

Formerly, Nagoya University, Nagoya, Japan e-mail<EMAIL_ADDRESS>
### **16.1 Introduction**

The sago palm, which originated in New Guinea Island, has created the sago culture that is the means of livelihood for local people where the palm occurs. The traditional dietary food culture of sago has developed under the conditions of different traditions of consumption and extraction of the starch. It is considered that the socioeconomic conditions determine the regional forms of sago extraction and use. Thus the changes in extraction technology have modified the forms of using sago. This subject was investigated in Indonesia where sago palm grows widely, extending from east to west. The factors relating to the various forms are also considered in this chapter.

The prototype of the starch extraction method is found in New Guinea and uses a hand ax type of pulverization of the palm pith and the hand-washing method for extraction of starch from crushed pith. Furthermore, the pulverization method was transformed through the following process modifications: hand ax or hatchet (sitting type), broadax (standing type), grater type (rasping model), and rasper (mechanization pulverization). Moreover, the starch extraction method, which washes pulverized pith, was also transformed as follows: the hand-washing type, the footwashing type, and the pump-use type (providing high pressure) (Nishimura 2015).

As for utilization, sago starch shifted from *ugari* as the staple food to various food uses. It is supposed that development from a staple food moved with the flow of confectionery (baked crackers, cookies) to noodles and to flour (substitution of other starch flour) (Hirao 2015). At present, sago starch as well as other starches can produce sugar and the materials for plastics through changing the starch character. The nature of these changes is related to the socioeconomics of production and consumption areas.

This paper clarifies the following points in consideration of the two factors of a geographical flow and time flow regarding the extraction method of sago starch. These are the change of method by geographical factors, change of consumption patterns of starch, and, in addition, the relationship between methods of change and the regional economy.

This study is based on results obtained from sago palm investigations in Indonesia conducted from 1992 to 2014. Moreover, some results of investigation from Mindanao, the Philippines, and Papua New Guinea are also included. The study concludes by incorporating results of the investigations in the field and interviews with people in the study areas.

### **16.2 Changes in Sago Starch Extraction**

The extraction technique of sago starch is an important task for sago-producing farmers; there are traditional extraction methods and technologies in each local area. It is recognized that there are regional differences even if the technology appears to be simple (Nishimura and Laufa 2002). This study examines the technologies or methods of sago starch extraction in Indonesia, a country extending for over 5000 km from east to west. As a result, the investigation found that there was a difference of the methods in New Guinea, which was the place of origin of a sago palm, and the western regions of Indonesia, to which sago spread. The difference of these methods has taken the form of technology transfer from the original area and a series of improvements in technology in each area.

The study analyzed in detail elements of the technology of four types: the New Guinea type, the Malay type, the intermediate type, and the mixed type as classified by Nishimura (2008b, 2012). From this analysis, enhanced investigations have been carried out, with the results shown in Table 16.1.

In New Guinea, a prototype of the extraction method (New Guinea type) was developed, and there are two forms for the pulverization of sago pith, sitting and standing. The tools used for this work of chopping are a sitting form using a hand ax (chopping ax/hatchet) and a standing form using a common ax (broadax). With the Malay type, which is a more developed type, the sitting form uses a hand ax as a basic form, and a grater form has also been developed. Moreover, the mechanization using raspers is progressing. The intermediate type is a sitting form using a hand ax. Moreover, in Mindanao, Philippines, there is a standing form involving a broadax considered as a mixed type (Nishimura 2008a).

The method of washing the mashed sago pith and extraction of starch exhibits regional differences like pulverization. The New Guinea type is a method in which water is poured in from the side by hand. More elaborate equipment may be made in some cases. In this case, the water flow is from the side (horizontal). Moreover, the Malay type is a starch extracting process which places the mashed pith into a basket where it is washed by foot action under pouring water. The water flow is vertical in this case. The intermediate type is the same as the Malay type which places the mashed pith into a basket and washing it by foot action under a vertical water flow. On the other hand, the method in Mindanao, Philippines, is the technology called the mixed type, and the flow of water is vertical although the mashed pith is washed by hand. Moreover, the mixed type which washes mashed pith by hand by

**Table 16.1** Grouping of the regional methods of sago starch extraction

Note:

Type/form: New Guinea T.; Intermediate F.; Malay T.; Mixed F.

Observed region: South Sorong; (K) Kendari, (B) Bogor; Riau; Mindanao

vertical water flow is seen as a peculiarity in Bogor, Java Island. In the case of comparison of these methods, origin/prototype and developed type, the pith pulverization went from a hand ax to a broadax and then a grater. Moreover, the method of starch extraction by washing in water has evolved from horizontal washing by hand (rubbing) to vertical washing by foot (crushing). Then, a mechanical motorized rasper came into use.

The local processing of sago palm is demonstrated using photographs (Fig. 16.1): the technical change of the pith-crushing work and washing (starch extraction) of the crushed pith, as currently performed in each area. In the case of diffusion of sago technology spreading from Papua Province, Indonesia, and New Guinea Island, the place of origin of sago palm, to the west, technology of the pulverization was transmitted from the east to the west changing to hand ax (sitting form), broadax (standing form), grater form (rasping model), and rasper (mechanization pulverization). Moreover, the method of washing crushed pith by water (starch extraction) changes, moving east to west similarly, going from hand to foot, and finally to the pump-use form. With the addition of a time factor, mechanization becomes technical development.

### **16.3 Changes in the Form of Starch Utilization**

Sago palm is an important crop, and the entire plant can be used by native Indonesians. The starch which is extracted serves as the staple food of people in the villages. It is clear that the areas of Indonesia which are located closer to New Guinea Island have a stronger dependence on sago as their staple food. In Kendari, Southeast Sulawesi, and South Sorong, West Papua province, a comparison was made between the staple food and other food. The results are shown in Table 16.2.

In the West Papua province, South Sorong district, and Metamani subdistrict, the staple food is sago, and it is eaten as *papeda* (porridge). There is also in their diet fish, shellfish, and wild animal meat, such as wild boar, deer, etc., obtained by hunting, as side dishes. On the other hand, in the Kendari district in Southeast Sulawesi, the staple food is rice and sago. Although rice as the staple food was grown as upland rice a long time ago, paddy rice is now cultivated. When indigenous people harvest rice, they eat it in the dry season; during the rainy season, they extract starch from the sago palm. Thus these two plants together provide their staple food. Side dishes in the diet are fish, shellfish, and wild animal meat, similar to West Papua. Cultivation of rice in Indonesia did not take place in the eastern part bordering Sulawesi (Takaya 1990). However, it can be seen that the movement of rice consumption as a staple food spread from the western to eastern regions where the main food is sago. Therefore, traditionally people in the eastern region most commonly consume sago starch as the staple food. Moreover, a unique use of sago starch is processed as noodles. Production of these noodles is mainly carried out in Semarang, Central Java. Since many Chinese immigrants have lived in Java since ancient times, production of the noodles as Chinese food was accomplished. However, sago starch is not produced in Semarang, and the sago starch used to make noodles is mainly brought from the Riau Province (commercialization). Moreover, confections are made as

**Table 16.2** Food situation in sago villages

a Kiaea village in Southeast Sulawesi province; observation was done in 1992 (Nishimura 1995) b Saga village in West Papua province, located in a wild sago forest. Observation was done in 2012

additional food. One form is *lempeng* (pancake), which is generally dried food, and can also be considered a preserved food. As well, cookies, shrimp crackers, sago pearls, etc. are made (Hirao 2015). Although confections are made and eaten by the farmers themselves, in many cases they are sold. Moreover, there are some people who make confections, especially in the towns. These forms change depending on regions, and in order to carry out sales, producers need to prepare a product suitable to meet the needs of local consumers.

According to the results of this study, the form of consumption of sago starch is classified into staple food, confections, starch flour, and biomaterial. Traditional farmers in sago palm areas consume sago starch as the staple food and as a confection. Depending on the developing rural economy, the use of sago is diversified and increasingly used as a confection and commercial starch. If the multiple use of this staple food progresses, it will shift from the use of sago starch to uses other than as a staple food. Looking at the usage of the sago starch regionally, diversification of the staple food is moving from east to west. That is, there is one staple food of sago in the provinces of Papua and Maluku to the east, but moving west to Sulawesi and the central islands, there are two staple food areas of rice and sago starch. Also, sago starch goes more to the development of confections and a commercial use to make noodles, such as in Java. Furthermore, in the Malay region on the western side of Kalimantan Province, it has shifted more to commercial starch use. This trend shows a change from east to west, similar to the change in sago starch extraction techniques. Therefore, the form of consumption of sago starch relates to the level of economic development of an area and to social change.

As for sago starch as a staple food, it is eaten in two forms, added to dishes such as soup or porridge, or as a dry food as a bread or biscuit. It is also consumed in the form of noodles made of sago starch. In confectionary form it is consumed as a specialty in Indonesia as crackers, cookies, or jelly. In traditional villages, the confectionery form is generally dry and consumed as a cracker. In addition, in a village on Mindanao Island, Philippines, the confectionery is made of sago starch fried in oil or steamed (Nishimura 2008a). Therefore, sago starch is important as a staple food in eastern Indonesia and consumed as a side dish or confectionery in the western part of the country. It is believed that this tendency is especially influenced by the Java culture which eats sweets (diversification of a meal). Furthermore, in the western Malay area, as commercialization progresses toward industrial uses such as starch flour, food use in the rural area of sago starch is being reduced.

### **16.4 Technical Flow and Economic Positioning**

It is believed that sago starch extraction technology spread to the western region of Indonesia from New Guinea, the place of sago origin. Extraction technology has improved into an appropriate form in each place over the process of this diffusion. The improved technological conditions are based on the development situation of sago villages. The production systems of sago starch differ in villages where sago is only a staple subsistence food and villages where sago is produced for sale. The rural socioeconomic situation becomes one of the factors for different forms of the production system. The economy of Java is the most developed in Indonesia. However, the economy is still underdeveloped elsewhere, especially in the eastern Indonesia islands. The economy and the social conditions of the study areas are shown in Table 16.3. Therefore, the socioeconomic conditions are still low for the areas of the eastern island region near the origin center of sago.

It is possible to consider how the starch extraction method currently found in each region has been changed from the prototype of New Guinea. The changing technology in an area, considering the form of the process from east to west, is shown in Table 16.4.

For the change of extraction technology, it is clear that the pulverization method of New Guinea of using an ax became a grater-type technology in and to the west of Sulawesi. In this development process, the use of mechanical raspers began. Similarly, also in the extraction technology, it changes from the hand-rubbing method which is the prototype to the more efficient foot-mashing method on Sulawesi Island in the western region. Also, pumping water under high pressure was introduced to this method, giving an improved and more efficient technology. However, the method of hand rubbing in Bogor is carried out by flushing water by gravity. This situation indicates that technology has developed toward the west from the east. This phenomenon is related to the social development situation of sago societies; economic conditions, especially, are a key factor in the development. That

Source: Statistic Indonesia (BPS), Financial Statistics (BPS) by OECF (1998)

**Table 16.4** Flow of the methods of sago starch extraction in Indonesia

is, the sago starch which is used only as a staple food is diversified for use in confectionery. The factor influencing the change in sago utilization is related to the background of the needs of consumers and markets. It is apparent that the greater diffusion of sago palms going toward the western regions, where there is a strong economy, the more diversification of sago utilization and extraction technology takes place. Therefore, the transformation in extraction and consumption process of sago starch depends on the development situation of the society and the economy in the regions.

### **16.5 Conclusion**

Sago starch extraction methods, pith pulverization and washing mashed pith by rubbing, changed their forms and diffused from place to place, spreading from the eastern regions. The changing factor of the method relates to the social economy and trade situation of the areas. The changes influence improvements toward practices that are more efficient and economical. In an area where the social economy and cashbased economy are developed, sago utilization shifts from staple food use to starch goods use. Commercialization of sago is determined by the result of comparison with the price of rice for staple food and other starch use for confectionery products.

Therefore, sago starch changes into a side dish of confectionery from a staple food, in areas of more developed economies. And sago has become the alternative (complementary) staple food of rice. Societies where sago became the staple food in the area do not have a developed economy, but sago becomes the alternative staple food in those more developed areas which have rice. It has already progressed as a food material for confectionery in the area in which it is no longer the staple food. Moreover, noodles are produced as a unique form of consumption and are considered to have been influenced by Chinese food culture. And it has changed in terms of the consumption needs from a subsistence food to a market product. The utilization and production forms of sago can be seen under the following circumstances:

The development circumstances of sago palm use in Indonesia have progressed from east to west. In order to shift development into commercialization from the stage of subsistence use of sago starch, the degree of socioeconomic development, consumption needs, and transportation development are indispensable factors. Moreover, it is simultaneously necessary to consider the time factor of the development standard of each area. Therefore, time flow (for the axis of regional development) becomes an important factor as well as regional factors for studying a technical change of the diffusion of the method. Therefore, it is necessary to take into consideration not only the changes in technology but also the time factor (development axis of the region) as well as the socioeconomic condition of a region for the full development of sago starch production.

### **References**

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### **Chapter 17 Improvement of Sago Processing Machinery**

**Darma**

**Abstract** The traditional method of sago starch extraction is a time- and laborintensive process. The most laborious stage is pith disintegration which is done by using a hammer-like tool called a pounder followed by washing and screening the starch. However, the use of mechanical processing equipment is saving time and energy. Consequently, sago starch production increased, both in quantity and quality. With regard to the mechanical processing, it is necessary to provide mechanical equipment which is suitable and easy to use by ordinary farmers. This paper provides an overview of improvement of small-scale sago processing machinery in order to improve the performance. It consists of two separate operation units, namely, the cylinder-type sago rasping machine and the stirrer blade-type sago starch extractor. The performance of the improved sago rasping machine is characterized by (a) rasping capacity 730–1009 kg/h, (b) starch percentage 47.2%, and (c) starch loss in sago pith waste of only 4%. Meanwhile, the performance of improved sago extraction machine is (a) extraction capacity 1007 kg of rasped pith per hour, (b) starch percentage was 24%, and (c) starch loss in waste is 2.1%. The machines are intended for small-scale (household) processing of sago and are suitable for adoption in most sago-producing areas, such as those in Papua and Papua New Guinea.

### **17.1 Introduction**

Indonesia has the largest potential of sago in the world, but the sago starch production and utilization are very small compared with its potential. According to Samad (2002), the utilization of sago palm resources in Indonesia is only about 0.1% of its total potential. Matanubun and Maturbongs (2006) stated that utilization of sago resources in West Papua, which has over 95% of Indonesia's sago palms, represents less than 5% of its existing potential. Up to the present time, farmers in this region cut sago palms and process starch mainly for subsistence use and to sell starch locally, but they exploit only a very small amount compared with its potential. Consequently, a large number of mature sago palm go unharvested and are lost

Darma (\*)

Faculty of Agricultural Technology, University of Papua, Manokwari, Indonesia e-mail<EMAIL_ADDRESS>
every year. Meanwhile the current demand for sago starch, both for local and global markets, continues to increase. There has been no significant increase in sago starch production in West Papua. Unlike in Sarawak, Malaysia, even though the sago potential is small, it was the world's largest exporter of sago starch with total exports of 44,700 mt in 2007 (Karim et al. 2008; Singhal et al. 2008; Bujang 2011). The sago industry in Malaysia (State of Sarawak) is well established and has become one of the important industries contributing to export revenue (Karim et al. 2008).

Traditional methods of sago starch extraction are now being used in most parts of West Papua, but mainly for subsistence. It is well known that the traditional method of sago starch processing is a time-consuming and labor-intensive process. Consequently, sago starch production is very low, both in quantity and quality. Farmers in the area continue to use traditional systems to process sago starch because they lack mechanical equipment. The industrial technology of processing starch and its derivatives from potato, cassava, maize, rice, and wheat is well developed. However, this is not the case with sago starch technology. There are only a few simple technologies besides the traditional method.

The principles and methods of sago starch processing or sago starch extraction are almost the same for both traditional and mechanical production, differing only in the equipment which is used and the scale of operation (Rajyalakshmi 2004; Kamal et al. 2007; Karim et al. 2008). The purpose of the extraction is to separate starch from the cellulosic cell walls of the trunk. This procedure is as follows: (1) palms are selected and felled; (2) clearing, debarking, and splitting the logs; (3) disintegration or breaking down the pith of the log; (4) starch extraction/separation; (5) starch sedimentation and dewatering; and (6) starch drying and packaging. The traditional method of sago starch extraction is not only ineffective and inefficient but also produces starch of low quality. In contrast, mechanical processing of sago palm pith, besides being much more effective and efficient, produces starch having higher quality and is more hygienic (Karim et al. 2008; Singhal et al. 2008). Therefore, farmers should change from the traditional method to the mechanical one in order to increase sago starch production. With regard to the mechanical processing, it is necessary to provide equipment that is suitable and easy to use by typical farmers. Mechanical processing of sago will transform the traditional agricultural system into a developed and commercial agriculture and result in an increase of farm income.

Mechanization in agriculture plays an important role because of its contribution in improving efficiency and productivity of agricultural resources. The application of technology in the form of appropriate machinery and equipment (appropriate technology) to the farmers in developing countries, such as Indonesia, is suitable to be applied. The characteristics of the technology should be simple, low in cost, small in scale, and labor-intensive. In addition, a region should have developed for it mechanical equipment suited to local conditions; consequently its application should not encounter any constraints. The application of mechanical equipment in some areas should pay attention to the various sociocultural aspects of the local community; otherwise mechanization will be unsuccessful. For instance, Sembiring et al. (1998) stated that the failure of agricultural mechanization in Sri Lanka was due to the application of imported agricultural machinery directly, unlike the Japanese who make modifications according to local conditions and then produce their own for use by their farmers. The sago processing equipment/machines to be improved and discussed in this paper are intended for small-scale (household) processing of sago starch because it was considered suitable for application in most sago-producing areas such as in Papua and Papua New Guinea. The mechanization consists of two separate operational units, cylinder-type sago rasper and a stirrer blade-type sago starch extractor.

### **17.2 Sago Processing**

The main edible food product obtained from sago palm is starch, which is stored in large quantities in its trunk as a prelude to flowering. The objective of sago processing is to extract starch from the sago logs. Sago palm is reported to be one of the cheapest and most readily available sources of food starch, with the highest productivity per land area among other starch crops (Bintoro 2011). There are several ways to extract the starch from the sago pith, but the principles and methods are similar. Traditionally, the starch extraction is performed manually by individual farmers or at domestic-scale sago processing plants. In contrast, modern processing is fully mechanized, has a relatively short processing time, and is more hygienic, as compared to traditional processing (Karim et al. 2008; Singhal et al. 2008). Principally, manual or traditional starch extraction is similar to the modern one, differing only in the scale of operation and the equipment used. In general, ready-to-harvest palms are selected and felled. The bark-like layer is stripped from the trunk, and it is cut into sections or floated whole to a central processing facility. There, it is, if necessary, cut into sections and reduced to battens and rasped either manually or mechanically to pulverize the pith and loosen starch particles within the fiber. The starch is removed from the fiber by kneading by hand or trampling by foot using water or by a spray of water. Starch-laden water or starch in suspension runs into a settling container, where the starch is precipitated out and the water overflows. The starch is then removed and dried.

### *17.2.1 Traditional Method of Sago Processing*

In most of the main sago areas throughout Southeast Asia and New Guinea, starch is extracted using the traditional method. This method is still commonly used in Papua New Guinea (Greenhill 2006), West Papua (Darma and Istalaksana 2011; Darma and Sarunggallo 2010, Darma and Kito 2014a, b), the Molucca Islands (Rumalutur 1992; Girsang 2014), and Seram (Ellen 2004). The traditional method is very labor-intensive and time-consuming, usually involving the cooperation of a small group of people or a family.