Abstract
The anatomical characteristics in the culms of the four promising Indonesian bamboo species, including Dendrocalamus asper, Dendrocalamus giganteus, Bambusa vulgaris var. vulgaris, and Bambusa vulgaris var. striata, were investigated to produce an identification key and quality indices for further effective utilization. The crystalline properties of the bamboo culm were determined using X-ray diffraction analysis. Dendrocalamus asper and Bambusa vulgaris var. striata showed vascular bundle type IV, while Dendrocalamus giganteus and Bambusa vulgaris var. vulgaris displayed vascular bundle type III. The vascular bundle density in the bamboo culms increased from the bottom to the top part and was higher in the outer part than in the inner part. The fiber portion and length in the outer part were higher than those in the inner part, opposite of those in the parenchyma portion. Dendrocalamus giganteus had the largest vessel and parenchyma diameter, while Bambusa vulgaris var. vulgaris had the smallest. Bambusa vulgaris var. vulgaris had the longest parenchyma, while Bambusa vulgaris var. striata and Dendrocalamus giganteus had the shortest. The outer part of the four bamboo culms showed higher relative crystallinity than the inner part. All anatomical parameters, except for crystallite width, showed a variation in the radial direction of the four bamboo culms but did not show a consistent tendency vertically. This study revealed that the anatomical properties were different between bamboo species and could be used for species identification and quality evaluation indices of the culms.
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Anatomical Characteristics for Identification and Quality Indices of Four Promising Commercial Bamboo Species in Java, Indonesia
Muhammad Iqbal Maulana,a,# Woo Seok Jeon,c,# Byantara Darsan Purusatama,d Jong Ho Kim,b Denni Prasetia,b Go Un Yang,b Alvin Muhammad Savero,b Deded Sarip Nawawi,a Siti Nikmatin,e,f Rita Kartika Sari,a Fauzi Febrianto,a,* Seung Hwan Lee,b and Nam Hun Kim b,*
The anatomical characteristics in the culms of the four promising Indonesian bamboo species, including Dendrocalamus asper, Dendrocalamus giganteus, Bambusa vulgaris var. vulgaris, and Bambusa vulgaris var. striata, were investigated to produce an identification key and quality indices for further effective utilization. The crystalline properties of the bamboo culm were determined using X-ray diffraction analysis. Dendrocalamus asper and Bambusa vulgaris var. striata showed vascular bundle type IV, while Dendrocalamus giganteus and Bambusa vulgaris var. vulgaris displayed vascular bundle type III. The vascular bundle density in the bamboo culms increased from the bottom to the top part and was higher in the outer part than in the inner part. The fiber portion and length in the outer part were higher than those in the inner part, opposite of those in the parenchyma portion. Dendrocalamus giganteus had the largest vessel and parenchyma diameter, while Bambusa vulgaris var. vulgaris had the smallest. Bambusa vulgaris var. vulgaris had the longest parenchyma, while Bambusa vulgaris var. striata and Dendrocalamus giganteus had the shortest. The outer part of the four bamboo culms showed higher relative crystallinity than the inner part. All anatomical parameters, except for crystallite width, showed a variation in the radial direction of the four bamboo culms but did not show a consistent tendency vertically. This study revealed that the anatomical properties were different between bamboo species and could be used for species identification and quality evaluation indices of the culms.
DOI: 10.15376/biores.17.1.1442-1453
Keywords: Bamboo anatomy; Bambusa sp.; Cell proportion; Dendrocalamus sp.; Crystalline properties; Vascular bundle type
Contact information: a: Department of Forest Products, Faculty of Forestry and Environment, IPB University (Bogor Agricultural University), Bogor 16680, Indonesia; b: Department of Forest Biomaterials Engineering, College of Forest and Environmental Science, Kangwon National University, Chuncheon 24341, Republic of Korea; c: Eagon Industrial Co., Ltd., Incheon, Republic of Korea 22107; d: Institute of Forest Science, Kangwon National University. Chuncheon 24341, Republic of Korea; e: Department of Physics, Faculty of Mathematics and Natural Sciences, IPB University (Bogor Agricultural University), Bogor 16680, Indonesia; f: Surfactant and Bioenergy Research Center, IPB University (Bogor Agricultural University), Bogor 16143, Indonesia; # The first two authors contributed equally to this work;
* Corresponding author: febrianto76@yahoo.com; kimnh@kangwon.ac.kr
INTRODUCTION
Bamboo is a multipurpose plant that provides many benefits. Ecologically, bamboo stands have a role in erosion control and riverbank protection (Osei et al. 2019). Bamboo is also used as a food and building material to provide social and economic value (Satya et al. 2010; Manandhar et al. 2019). Recently, interest in bamboo utilization has increased alongside the demand for alternative wood and lignocellulosic raw materials. Several studies have reported the use of bamboo culm in various products, such as bioenergy (Park et al. 2018, 2019), composite materials (Febrianto et al. 2012, 2015; Maulana et al. 2021a), and nanocellulose materials (Jang et al. 2020; Rasheed et al. 2020).
The diversity of bamboo species provides a challenge in determining the appropriate use of bamboo species. A total of 1642 bamboo species from 75 genera have been identified worldwide (Vorontsova et al. 2016). There are 161 bamboo species from 12 native genera in Indonesia, including Dendrocalamus, Bambusa, Gigantochloa, Schizaostachyum, Nastus, Dinochloa, Fimbribambusa, Neololeba, Pinga, Racemobambos, Sphaerobambos, and Parabambusa (Widjaja et al. 2014). The classification of species and genera of bamboo is mainly based on the morphology of its reproductive structure (Clark et al. 2015). This allows species in the same genus to have different anatomical characteristics and species with similar anatomical characteristics to be grouped into different genera. In addition, the physical and mechanical properties of bamboo could be influenced by its anatomical characteristics; therefore, studying the anatomical characteristics of bamboo culms is essential.
Anatomically, the bamboo culm tissue is mostly parenchyma and the vascular bundles. The vascular bundles are composed of vessels, sieve tubes with companion cells, and fibers. The cell compositions of the bamboo culm are about 50% parenchyma, 40% fiber, and 10% conducting tissues (vessels and sieve tubes) with some variation according to species (Liese 1987). Moreover, the anatomical characteristics of bamboo also vary within culms, such as in the radial and axial directions.
There are several studies on the variation of anatomical characteristics within the bamboo culm. Huang et al. (2015) mentioned that the larger vascular bundles and parenchyma lumen diameter are located in the middle zone of Bambusa rigida, and the longer fiber and parenchyma are also found in the middle zone. The vascular bundle size, vessel lumen diameter, fiber lumen diameter, parenchyma length, and lumen decrease with increasing height. Sharma et al. (2017) reported that the vascular bundle of Schizostachyum manii, Schizostachyum munroi, and Schizostachyum pergracile are larger in the middle zone of the bamboo culm. In addition, the authors revealed that the vascular bundle density increases across the bamboo culm, while the fiber dimension and the wall thickness decrease. Jeon et al. (2018a) mentioned that vascular bundle density, fiber length, and the relative crystallinity in the three species of Phyllostachys bamboo are higher at the outer part than the inner part of the culm. Darwis et al. (2020) reported that the fiber length of Gigantochloa pruriens is the greatest in the middle part and smallest in the bottom part. Maulana et al. (2021b) mentioned that the vascular bundle density, fiber length, and relative crystallinity of three Gigantochloa bamboo culms from Indonesia are higher in the outer part of the culm than the inner part.
The four bamboo species Dendrocalamus asper, D. giganteus, Bambusa vulgaris var. vulgaris, and B. vulgaris var. striata are native to Indonesia. These types have many uses and potential as alternative raw materials for the wood industry. Dendrocalamus asper has been used for large structure building and furniture because it has good strength and does not easily crack when drying (Minke 2011). Dendrocalamus giganteus has potential in structural composite materials and bio-charcoal (Sun et al. 2020, Park et al. 2020). Bambusa vulgaris var. vulgaris has been widely cultivated as the raw material for pulp and paper in Brazil (Júnior et al. 2019). Meanwhile, Bambusa vulgaris var. striata has long been used as a temporary building material in Balinese traditional ceremonies (Arinasa and Bagus 2010).
Although these bamboo species have been used in various applications, the anatomical characteristics of these bamboos are rarely reported. In addition, there has been no study on the radial and axial variation of anatomical characteristics in Dendrocalamus asper, D. giganteus, Bambusa vulgaris var. vulgaris, and B. vulgaris var. striata. Therefore, the anatomical characteristics of D. asper, D. giganteus, B. vulgaris var. vulgaris, and B. vulgaris var. striata culms in the radial and axial direction were investigated in order to enrich the information regarding species identification and further utilization.
EXPERIMENTAL
Materials
Three culms each from five-year-old bamboo specimens of Dendrocalamus asper, Dendrocalamus giganteus, Bambusa vulgaris var. vulgaris, and Bambusa vulgaris var. striata were collected from the bamboo garden of the Research and Development Center (P3) Biomaterials, Indonesian Institute of Sciences, Cibinong, Bogor, Indonesia (6° 29′ 43.2″ S, 106° 51′ 11.9″ E). The stems were cut at the second node above the ground, and the branched tops were removed, leaving three-quarters of the total height of the stem. These stems were divided into three parts with equal length, consisting of the top, middle, and bottom (SNI 8020: 2014 2014). Detailed information on the four bamboo materials is shown in Table 1.
Table 1. General Information of Four Bamboo Species
Optical Microscopy
Bamboo blocks (10 (L) x 10 (R) x 10 (T) mm3) were softened in a boiling mixture of glycerin and water (50:50). Thin slices with a 15 to 20 µm thickness from the cross, radial, and tangential sections were prepared with a rotary microtome (Leica RM 2165, Heidelberg, Germany). The sections were then stained with 1% safranin solution and 1% light green SF yellowish solution. Next, the stained sections were dehydrated using an ethanol series (50%, 70%, 90%, 95%, and 99%) and xylene (Jeon et al. 2018a). Permanent slides were made using Canadian balsam resin. For fiber length measurement, match-sized bamboo strips were macerated with a mixed solution in a 1:1 (V/V) ratio of glacial H2O2 and CH3COOH at 60 °C until they were defibrillated (Franklin 1945).
In this study, the density of the vascular bundle was measured in a 4 mm2 area. The cell proportion was determined as the ratio of the area of each cell type to the total area using optical micrographs at 4x magnification. Data on vascular bundle density and cell proportion were collected 10 and 5 times, respectively. The dimensions of fiber, vessel, and parenchyma cells were measured from 40 replications. Vascular bundle type, vascular bundle density, fiber length, parenchyma dimensions, vessel diameter, and cell proportion were observed using an optical microscope (Nikon Eclipse E600, Tokyo, Japan) and an image analyzer (IMT i-solution lite, Version 9.1, Vancouver, Canada).
X-ray Diffraction Analysis
Equatorial X-ray diffractograms of the bamboo culms were taken via reflection mode using the X-ray diffraction apparatus (Cu target, DMAX 2100V, Rigaku, Tokyo, Japan, 40 kV, 40 mA) installed at Kangwon National University, Chuncheon, Korea. The Segal method (Segal et al. 1959) and Scherrer equation (Burton et al. 2009) were used to analyze the relative crystallinity and crystal width of the cellulose in the bamboo culms.
Data Analysis
Analysis of variance (ANOVA) and Duncan’s Multiple Range Test were applied to test the significance of vascular bundle density, cell dimension, cell proportion, and crystalline properties of the bamboo culm using IBM SPSS Statistics, Version 21 (IBM, Armonk, USA).
RESULTS AND DISCUSSION
Characteristics of the Vascular Bundle
Figure 1 shows the vascular bundles type of the four bamboo species in Dendrocalamus and Bambusa genus. D. asper and B. vulgaris var. striata exhibited a type IV vascular bundle, while D. giganteus and B. vulgaris var. vulgaris exhibited a type III vascular bundle. The vascular bundle of bamboo was distinguished into four types based on the central vascular strand pattern and the number of fiber strands (Grosser and Liese 1971). The vascular bundle type III consists of one central vascular strand and one fiber strand. Additional fiber strands were outside the central vascular strand and were distinguishable from vascular bundle type IV from type III.
Fig. 1. Vascular bundles in the cross sections of D. asper (A), D. giganteus (B), B vulgaris var. vulgaris (C), and B. vulgaris var. striata (D); VCS: vascular central strand, Pa: parenchyma cells, FS: fiber strand, MX: metaxylem vessels, Ph: phloem
Vascular bundles type III and IV are common in tropical bamboo species and can be found in Dendrocalamus and Bambusa (Grosser and Liese 1973). These vascular bundles are quite different from the vascular bundle types I and II, which only consist of central vascular strands. Vascular bundle type I was found in subtropical bamboos with leptomorph rhizomes, such as Phyllostachys pubescens (Jeon et al. 2018b). Sharma et al. (2021) found the vascular bundle type II in the bamboos with pachymorph rhizomes such as Cephalostachyum mannii. They also suggested that species within the same genus may have different types of vascular bundles. Similar results were reported by Sharma et al. (2017) on some Schizostachyum species, where Schizostachyum manii had vascular bundle type I, while Schizostachyum pergracile had vascular bundle type II.
As shown in Table 2, the vascular bundle density was also significantly different among species. Bambusa vulgaris var. vulgaris had the highest vascular bundle density, while D. asper had the lowest. In the radial direction, the vascular bundle densities in the inner parts of the four bamboo species were significantly lower than those in the outer part of the bamboo culm. In the axial direction, the vascular bundle density showed a tendency to increase from the bottom to the top. A similar trend on the variation of vascular bundle density was reported in the bamboo culm of the same genus. Huang et al. (2015) reported that the frequency of vascular bundle in Bambusa rigida increased from the inner part to the outer part and from the bottom part to the top part. Additionally, a higher vascular bundle concentration in the outer and top parts was found in Dendrocalamus brandisii (Wang et al. 2016). In our previous study (Maulana et al. 2021b), the vascular bundle density in Gigantochloa bamboo from Indonesia was higher in the outer part than in the inner part, while there was no variation in the axial direction of the bamboo culm.
Table 2. Vascular Bundle Density in Four Bamboo Species (Unit: umber/4 mm2)
Cell Proportion
The cell portions of fiber, parenchyma, and vessel in the four bamboo species are shown in Table 3. There are significant differences found in cell proportion between the genera. Bambusa species had a higher fiber proportion and lower parenchyma proportion compared to Dendrocalamus species. The vessel proportion in the inner part of the Dendrocalamus species was lower than that of the Bambusa species. In the outer part, D. asper yielded a higher fiber proportion than D. giganteus, while there was no significant difference between Bambusa species. In the inner part, B. vulgaris var. striata had a higher fiber proportion than B. vulgaris var. vulgaris, while there was no significant difference between D. asper and D. giganteus. The parenchyma proportion in the outer part of D. asper was significantly lower than that of D. giganteus, while B. vulgaris var. striata had a higher parenchyma proportion than B. vulgaris var. vulgaris. In the inner part, D. asper had a significantly higher parenchyma proportion than D. giganteus, and there was no significant difference between Bambusa species. The vessel proportion in the outer part of D. asper was significantly higher than that of D. giganteus, and B. vulgaris var. striata yielded a higher vessel proportion than B. vulgaris var. vulgaris.
The fiber proportion in the outer part of the bamboo culm was higher than that in the inner part, while the parenchyma had higher proportions in the inner section than the outer section. Vessel proportions in the inner part were higher than those in the outer part except for D. asper. The vessel proportion increased from the bottom to the top section of the bamboo culm. However, the fiber and parenchyma proportions did not show a fixed trend in the axial direction.
The cell proportions within the bamboo culm in this study were in line with those of the three Gigantochloa species (Maulana et al. 2021b). The radial variation in the cell proportions could be caused by the radial variations in vascular bundle density. As Huang et al (2015) mentioned, the higher the vascular bundle density in the outer part of the bamboo culm, the lower the parenchyma proportion. In addition, Darwis et al. (2020) reported that the vascular bundle percentage of Gigantochloa pruriens increased from the inner to the outer part, while the opposite was true for the parenchyma percentage.
Table 3. Cell Portion of the Four Bamboo Species (unit: %)
Cells Dimensions
Table 4 shows the fiber length in the culms of four bamboo species. In the outer part, there was no significant difference between the fiber lengths of Dendrocalamus species. In addition, B. vulgaris var. striata had greater fiber length than B. vulgaris var. vulgaris. In the inner part, the fiber length was similar between Dendrocalamus species, while B. vulgaris var. striata had greater fiber length than B. vulgaris var. vulgaris. Moreover, Dendrocalamus had longer fibers than Bambusa, while Bambusa vulgaris var. vulgaris had the shortest fiber among the four bamboo species.
The fiber length in the outer part was significantly higher than that in the inner part. A similar trend in the radial direction was reported on the bamboos of Phyllostachys (Jeon et al. 2018a) and Gigantochloa (Maulana et al. 2021b). The middle part of the bamboo culm had the longest fiber in the axial direction, except for the inner part of the culm in B. vulgaris var. vulgaris. In the axial direction, Kumar et al. (2015) previously reported that the middle culm of Bambusa mizorameana had the longest fiber. On the other hand, the fiber length of Dendrocalamus brandisii decreased from the bottom to the top of the bamboo culm (Wang et al. 2016).
Table 4. Fiber Length of the four Bamboo Species (Unit: µm)
The optical micrographs of the radial and tangential sections in the four bamboo species used for measuring dimensions of vessel and parenchymal cells are shown in Fig. 2. The dimension of the vessel and parenchyma of the four bamboo species are presented in Table 5.
Fig. 2. Optical micrographs of radial (1) and tangential (2) sections of D. asper (a), D. giganteus (b), B. vulgaris var. vulgaris (c), and B. vulgaris var. striata (d). Pa: parenchyma cells, MX: metaxylem vessel, Fb: Fiber bundle
There were significant differences in the vessel diameter and parenchyma dimension between species. Dendrocalamus giganteus had the largest vessel and parenchyma diameter, while B. vulgaris var. vulgaris presented the smallest. Even though they are from the same genus, B. vulgaris var. vulgaris had the longest parenchyma while B. vulgaris var. striata had the shortest parenchyma. There was no significant difference in parenchyma length between the tangential and radial sections. Sharma et al. (2011) reported that the vessel width in D. hamiltonii, B. tuda, B. balcooa, and B. aurandacea from India ranged from 34.4 to 48.4 µm, which are smaller than the values measured in this study. They also reported lower values of parenchyma width and length compared to the results of this study. The vessel diameter in this study was also larger than that of the three Phyllostachys bamboos from a subtropical area, ranging from 90.9 to 117.9 µm (Jeon et al. 2018a).
Table 5. Dimension of Vessel and Parenchyma of the Four Bamboo Species
Crystalline Properties
The relative crystallinity and crystallite width of the four bamboo species are shown in Table 6. There were some differences in the crystalline properties between the bamboo species. Bambusa vulgaris var. vulgaris showed the highest relative crystallinity and crystallite width, while D. giganteus had the lowest values. The crystallite width and relative crystallinity in the inner part were lower than those in the outer part of the culms.
Table 6. Crystalline Properties of the Four Bamboo Species
The crystalline properties such as relative crystallinity and crystallite width defined the portion and size of crystalline in cellulose, and these properties are essential for species identification and evaluation of bamboo quality. Besides, relative crystallinity was one of the indices that affected the mechanical and physical properties. There are studies that have reported on radial variation in the relative crystallinity and crystallite width of bamboo species. Jeon et al. (2018a) reported that the relative crystallinity of three Phyllostachys bamboos decreased from the outer part to the inner part. The relative crystallinity and crystallite width in the outer part of three Gigantochloa bamboos were also higher than those in the inner part (Maulana et al. 2021b). The crystallite width of four bamboo species in this study seemed lower than that in other studies: 5.59 nm in Dendrocalamus asper (Fatriasari et al. 2014) and 5.70 nm in Bambusa vulgaris (Brito et al. 2012).
CONCLUSIONS
- Dendrocalamus asper and Bambusa vulgaris var. striata presented vascular bundle type IV while D. giganteus and B. vulgaris var. vulgaris displayed vascular bundle type III. Vascular bundle density in the bamboo culms increased from the bottom to the top portion and was higher in the outer part than in the inner part.
- The outer part of the bamboo culm had a higher fiber portion than the inner part, and vice versa was observed in the parenchyma portion. The vessel proportion in the inner part of the Dendrocalamus species was lower than that of the Bambusa species.
- The fiber length in the outer part of bamboo culm was significantly higher than that in the inner part. Dendrocalamus species had longer fibers than Bambusa species. D. giganteus had the largest vessel and parenchyma diameters, while B. vulgaris var. vulgaris had the smallest.
- The outer part of the bamboo culm showed slightly higher relative crystallinity and crystalline width than the inner part.
- All parameters showed a variation in the radial direction of the of the four bamboo culm but did not show a consistent tendency in the axial direction.
- Finally, there were significant differences in anatomical characteristics between the bamboo species. It has been suggested that the results of this study could be used for the identification and quality indices of the bamboo species.
ACKNOWLEDGMENTS
The authors acknowledge the World Class Research (WCR) (No. 2345 /IT3.L1 /PN /2021) and Basic Research (PD) (No. 2039 / IT3.L1 /PN /2021) Grants from Deputy of Strengthening for Research and Development, Ministry of Research and Technology/National Research and Innovation Agency, Republic of Indonesia for to the financial support. This study was also supported by the Science and Technology Support Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (MSIT) (NRF-2019K1A3A9A01000018) and the Basic Science Research Program through NRF funded by the Ministry of Education (No. 2016R1D1A1B01008339 and 2018R1A6A1A03025582). Finally, we would like to thank Editage (www.editage.co.kr) for English language editing.
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Article submitted: October 6, 2021; Peer review completed: November 6, 2021; Revised version received and accepted: December 16, 2021; Published: January 11, 2022.
DOI: 10.15376/biores.17.1.1442-1453