1412-033X (printed edition) ISSN: 2085-4722 (electronic)

ISSN: 1412-033X (printed edition) ISSN: 2085-4722 (electronic)

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BIODIVERSITAS ISSN: 1412-033X (printed edition) Volume 11, Number 4, October 2010 ISSN: 2085-4722 (electronic) Pages: 167-175

Anatomy and morphology character of five Indonesian banana cultivars (Musa spp.) of different ploidy level

ISSIREP SUMARDI♥, MERA WULANDARI Faculty of Biology, Gadjah Mada University (UGM), Jl. Teknika Selatan, Sekip Utara, Sleman, Yogyakarta 55281, Indonesia. Tel. & Fax: +62-0274-

580839, ♥email: [email protected]

Manuscript received: 6 July 2010. Revision accepted: 18 October 2010.

ABSTRACT

Sumardi I, Wulandari M (2011) Anatomy and morphology character of five Indonesian banana cultivars (Musa spp.) of different ploidy level. Biodiversitas 12: 167-175. In Indonesia there are many cultivars of banana, and some of them produce edible fruits. Beside their morphology, the character which necessary as a tool for classification is anatomical character. The aim of this research were to describe the anatomical character and morphology of fives Indonesian banana cultivars based on their level of ploidy. The cultivars were collected from Banana Germplasm Plantation, Yogyakarta District, Indonesia. The samples of roots, rhizome, and leaf were collected from five banana cultivars i.e.: Musa acuminata cv Penjalin, M.balbisiana cv Kluthuk warangan, M.acuminata cv Ambon warangan, M.paradisiaca cv Raja nangka , and M. paradisiaca cv Kluthuk susu. For anatomy observation samples were prepared using paraffin method, stained with 1% safranin in 70% ethanol. To observe the structure of stomata and epidermis surface, slide were prepared using modification of whole mount method. Slides were observed using Olympus BHB microscope completed with Olympus camera BM-10A. Stem and leaf morphology character of diploid level (AA and BB genome) is different with triploid level (AAA, AAB, and ABB genome). Anatomy and morphology character of root and rhizome of banana in diploid level (AA and BB genome) and triploid level (AAA, AAB, and ABB genome) is quite similar. Distribution of stomata is found in leaf and pseudostem. Stomata is found in adaxial and abaxial epidermis layer. The size of guard cells in triploid cultivars was longer than that diploid cultivars. The root composse of epidermis layer, cortex and cylinder vascular of five cultivar’s root show anomalous structure. Rhizome consist of peripheric and centre zone. Anatomically, this was no differences in the rizome structur among five banana cultivars. The row of vascular bundles act as demarcation area between peripheric and central zone. In the cultivar with BB genome (diploid) and ABB genome (triploid) the row of vascular bundle was not found. The differences of leaf anatomy were base on: size and number of stomata distribution, number of subsidiary cells, number of hypodermal layers, structure and number of parenchyma palisaden, size of airspace in petiole and mesophyll and the vascular bundle structure.

Key words: anatomical character, morphology, banana cultivar, ploidy level.

INTRODUCTION

Bananas are among the largest herbs in the world. They are perennials with tall aerial shoots that arise from swollen, fleshy corms. The distribution of species is influenced by morphology, chromosome number and geographical location (Wang et al. 2010). Nowadays the existing banana in many country was supposed as a line of Musa acuminata Colla and M. balbisiana Colla (Simmonds 1959). The line species are diploid (AA genome), triploid (AAA genome) and tetraploid (AAAA genome). Banana plants have various ploidy level, as a result of natural crossing between wild species continuously and the effect of environment. These process cause the rise of new species with different ploidy level, i.e.: diploid, triploid and tetraploid. Crossing between M. acuminata (AAAA genome) and M. balbisiana (BB genome), for example, resulting triploid level with genome symbol AAB or ABB (Purseglove 1979). Caryotype and number of chromosom are generally very importance in studying classification, but the chromosom number is not absolutely as a case, because some species of plant that have same chromosom

number perform different character. M. acuminata (AA genome, 2n=22) produce edible fruit, but M. balbisiana (BB genome, 2n=22) has many seed and not edible fruit (Fitri 2007).

Cheung and Town (2007) reported in order to view the sequence composition of the M. accuminata in a cost effective and efficient manner, 6.252 of BAC (Bacterial artificial Chromosomes) gen sequences were search again several data bases, and significant homology was found in mitochondria, chloroplast, and protein. Wang et al. (2010) compare 20 sugarcane BAC with sorghum sequencing to know the character of complex autopolyploid sugarcane at the DNA sequencing level. The complexity of the aupoliploid genome at the interspecific hybridization of modern cultivar hindered progress in genetic research and the application of genomic tool in breeding programe (D’Hont 2005). Recent genome and molecular cytogenetic data provided cytogenetic evidence that some species were derived from interspecific hybridization between two different species (D'Hont et al. 2002).

The line species from M. acuminata and M. balbisiana crossing is M. paradisiacal Linn. Biodiversity of banana

BIODIVERSITAS 11 (4): 167-175, October 2010

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cultivar are caused by natural crossing or somatic mutation proceed for along time (Stover and Simmonds 1987) or caused by the selection and vegetative propagation (Purseglove 1979). The diversity of banana could be differentiated by the taste, shape and color of fruit. The species and cultivar of banana which to be found in Indonesia have not all been classified yet. Molecular approach and chromosome caryotype have been used to determine the phylogenetic relationship among some species of bananas (Retnoningsih 2009). Kustanti (2005) studied the relationship of Belo bamboo with three bamboo genera based on their stem anatomy. Wardhana et al. (2009, pers. comm.) worked with some species of yams tuber to determine their relationship based on tuber anatomy. Anatomy traits were selected from previous report of phase-specific in maize (Bongard-Pierce et al. 1996) and in three grasses plants: maize (Zea mays L.), rice (Oryza sativa L.) and bluegrass (Poa pratensis L.) (Sylvester et al. 2001). The traits included epidermis cell shape, the precense and abcense of epicuticular wax, hairs, stomata and bulliform cell.

Anatomy knowledge is essential when vegetative propagation is used to identify important structural feature necessary for propagation success (Silva-Lima et al. 2005). Information on anatomical structure is needed by breeder working on improvement for drought tolerance (Nassar et al. 2008). Using 0.2% colchicine they found various ploidy level in cassava plant. Tetraploid type in cassava show more prismatic and druse crystal in the cortical parenchyma, pericycle fibers had thickening wall, secondary xylem was wider than diploid one, which having thinner walls and less starch.

The aims of this research were to examine the morpho-logical and anatomy characters of five Indonesian banana cultivars found in Yogyakarta based on their ploidy level. These character is very important as supporting data for classification.

MATERIAL AND METHODS

Plant materials. Samples were collected from Banana Plantation in Yogyakarta District, Indonesia. The five cultivars were: M. acuminata cv Penjalin (AA genom), M. balbisiana cv Kluthuk warangan (BB genom), M. acuminata cv Ambon warangan (AAA genom), M. paradisiaca cv Raja nangka (AAB genom) and M. paradisiaca cv Kluthuk susu (ABB genom). The morphological character included root, rhizome, pseudostem, leaf and plant habit. For anatomical characters: root, rhizome, pseudostem, leaf blade and midrib, shape, size and distribution of stomata in epidermis layer and pseudostem were observed.

Morphology. Morphology characters observed were: root, growth of adventitious root, rhizome color, pseudostem color, leaf blade, shape and size of midrib and plant habitus.

Anatomy. In order to analyze of vegetative structures, samples (root, rhizome, leaf blade, petiole, and pseudostem) were prepared using paraffin method, while epidermis layer of leaf and pseudostem were processed using modification of whole mount method (Ruzin 1999).

Paraffin method procedure. Material was fixed in FAA (90 mL ethanol 70%, 5 mL acetic acid, and 5 mL formaldehyde 36%) solution; (ii) the materials were washed repeatedly in 70% ethanol and dehydrated with ethanol series (80%, 90% and 95%); (iii) sequently dealcoholization step using absolute ethanol and xylene mixture i.e.: ethanol/xylene 3: 1; 1: 1; and 1: 3 (iv) infiltration step: the mixture of ethanol/xylene was replace with the mixture of liquid paraffin and xylene (9: 1), for 24 hours; (v) embedding step: before embedding step, the material was immersed in pure liquid paraffin for one hour and then embedded using the pure paraffin (560/570C); (vi) The embedded sample were sectioned in thinly slide using rotary microtome. The sliced sample were stained with 1% safranin in 70% ethanol; (vii) after staining, the slides were observed under the Olympus microscope and the photograph were taken using the Olympus BHB Model completed with Olympus Camera BM-10A.

Whole mount methode. the peeling of leaf epidermis layer and pseudostem each were immersed in chloral-hydrate (250 g/100 mL) for short time until the material became transparent; (ii) the samples were then washed two to three times in distilled water to remove the trace of chloralhydrate, and stained the material with 1% safranin in distilled water for 20 minutes; (iii) the material were washed repeatedly with distilled water; (iv) the materials then were put in slideglass and small drops of the glycerine were added to the slides and covered with coverslip; (v) the slides were observed under Olympus microscope and photograph were made using microscope like above

RESULT AND DISCUSSION

Morphology Root of the five cultivars perform quite similar in

morphology character behavior (Table 1). The young roots showed white color, and became brown in mature roots. Many root hairs were found on the surface of root.

Stem of the five cultivars were different in stem diameter and pseudostem color. The true stem was formed when the plant started to form reproductive organ. The pseudostem was formed as the modification of the lower part of the midrib. Pseudostem had red, yellowish green and reddish green color. On the basal part of the stem big structure called rhizome was found.

Leaf of banana was belonging complete type group, because they had midrib, petiole and leaf blade. The modification of basal part of midrib was called pseudostem. The petiole had halfcircle-like shape and the adaxial part grooved. The shape of leaf blade was oblonge with flat tip. The abaxial and the adaxial suface of leaf were protected by cuticle layer. The cutin layer was also found in the petiole. The five cultivars studied formed green leaves with nearly the similar size.

General anatomy Root of all five cultivars have similar structure, which

consist of three tissue systems, epidermis, ground parenchyma and vascular cylinder.

SUMARDI & WULANDARI – Anatomy and morphology characteristic of banana

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Cortex. of mature roots had many layers with thick-walled cells in outside surface. According to Tomlinson (1969) those tissues were periderm. This tissues was a protected layer. Young root of cultivar Penjalin and Raja nangka have one to two epidermis layers. Cortex composed of parenchyma cells, with many and big airspace. The shape of parenchyma cells were irregular. The big airspace became larger in size. Swennen and Oritz (1997) called it lacunae. The large airspace in several species of monocotyledon may have schizogenous or lysigenous in origin. But sometime it may arise by combination of the two processes (Esau 1978). Airspace of some roots is regarded as a serving tissue in gas transport, because airspace as reservoir of oxygen, which is required in the respiration by the tissue which have no acces to the oxygen of the air (Fahn 1990). From five cultivars, only Raja nangka cultivar have no airspace.

Endodermis. the boundary layer between cortex and vascular cylinder, consist of one layer which composed of thick cell. The cell wall of endodermis have U-like shape thickening (Esau 1978; Raven et al. 1999). This wall composed of suberin and cellulose. At first thickness of the endodermis was like strip, and then developed into a band, called Casparian band (Esau 1978). The endodermis cells continuosly thickened, and finally the shape of band changed to the U shape. Suberin and cellulose materials deposited radially and tangensially in inner side wall. This condition was found in Penjalin, Kluthuk warangan, Ambon warangan and Kluthuk susu cultivar, while the structure of endodermis in Raja nangka cultivar was not similar with the others.

Pericycle. the outer layer of vascular cylinder was called pericycle. It was a single layer, and compossed of meristematic cells. In mature root the function of this layer was to form adventitious roots (Fahn 1990). Some root of five cultivars showed primordial of adventitious root which originated from the pericycle. As example, roots of Penjalin cultivar, Ambon warangan, and Raja nangka.

Vascular cylinder (stele). Generally vascular system in monocotyledons is radial. In banana the vessels scattered at the center of root. The phloem cells were formed alternately with vessel cells in the perifer side of cylinder, and no pith was found. Generally in monocotyledonous root, xylem frequently forms a solid core with ridgelike projections, and strands of phloem alternate with the xylem ridge (Esau 1978). In banana root phloem widerspread between the vessels in the center. In root of Kluthuk warangan, some of vessels were surrounded by tracheid cells. So the arrangement of phloem irregular in the central zone, and xylem did not form ridge-like structure as found generally in monocotyledonous root. This condition showed the anomalous structure (Figure 1). This result contributed by Tomlison (1969) supposed, that the development of banana root showed anomalous structure. According Swennen and Oritz (1997) the formation of xylem in banana root will stop when the root stop to elongate. Root parenchyma compossed of thick wall cells.

Laticifer. Laticifer were scaterred in the cortex and vascular cylinder zone of five banana cultivars root. Laticifers are cells or series of connected cells that contain

latex, a fluid or complex composition substances. Banana laticifer was clearly colorless, like milk or brown color. In Musaceae, laticifer the compound type which were derived from series of cells. The series of cells in compound laticifer become united by dissolution of intervening walls. By this junction the laticifer cells compound developed wall perforation and this structure was called articulate (Nugroho et al. 2003). The type of laticifer in all banana cultivars were compound type and non anastomosis. The differences of five cultivars root can be seen on Table 1.

Anatomy of rhizome and pseudostem Cross section

Rhizome. The basal part of banana stem is rhizome. Rhizome grew after reproductive organ were formed as modification of the peduncle, white in color, with smooth surface. Rhizome consists of epidermis, pheriphery zone and center zone.

Epidermis. It was a single layer, dense cells, without intercellular space. In mature rhizome, many layer of periderms were found beneath the epidermis. In rhizome there were no cortex like those in monocotyledons stem. In Monocotyledonous stem there are no cortex as well as stele because no demarcation between both area (Nugroho et al. 2006 and Esau 1978). Rhizome of the five banana cultivars consist of two zones, i.e.: periphery zone and central zone.

Pheriphery zone. It consisted of parenchymatic cells and small vascular bundles, with no partition between central zone. The shape of parenchymatic cells in pheriphere were irregular and small. The pheriphery zone was narrower than central zone. Small vascular bundle were scattered in the pheriphery zone. The xylem of vascular bundle consists of vessel cell and not all of bundle was protected by thick wall tissues.

Central zone. It consisted of irregular parenchymatic cells, which was wider compared with the periphery zone. Vascular bundle were scattered and their number were quite frequent. The partition between central and peripheric zone generally marked by the row of vascular bundles which made them close regularly. The type of vascular bundle was close-collateral, because no cambium layer between xylem and phloem were formed. The size of vascular bundle in central zone was bigger than in the pheriphery zone. In the part of the central zone the vascular bundles were even bigger. The xylem consist of vessel only, with thick wall. The phloem with thin wall, gathered in the side of vessel cells. The bundle was not protected by sheath. The size, structure, and diameter of vascular bundle were varied among five banana cultivars, and this variations were depended on the ploidy level. Cytological work by de Azkue and Martinez (1990) found a group of a dozen morphiologically similar Andean species that share a base of chromosome number of x=8 which is rare in Oxalis. Base of chromosome numbers Oxalis vary from x=5 to x=12, with x=7 most frequent, and polyploidy is common in the genus (Emshwiller and Doyle 1998).

Laticifer. Laticifer were found in rhizome of five banana cultivars. Laticifers were rounded by the parenchymatic cells. The structure of rhizome laticifer was similar with that of root laticifer. The location of laticifer


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Table 1. Root and rhizome morphology and anatomy characters of five Indonesian banana cultivars of different ploidy level

Character Cultivar

Penjalin (AA) Kluthuk warangan (BB)

Ambon warangan (AAA)

Kluthuk susu (ABB)

Raja nangka (AAB)

Root Morphology Root type Fibrous Fibrous Fibrous Fibrous fibrous Root color Young: white Young: white Young: white Young: white Young: white

Mature: brown Mature: brown Mature: brown Mature: brown Mature: brown Anatomy Epidermis Number 1-2 layers 1 layer 1 layer 1 layer 1-2 layers

Cortex Shape of parenchyma 4-8 sides Irregular Irregular Irregular-four sides 4-8 sides Airspace Radial radial Radial Radial No airspace Pericycle 1 layer 1 layer 1 layer 1 layer 1 layer

Cylinder vascular Xilem

Protoxylem in peripher, metaxylem scattered

protoxylem and meta-xilem were rounded by thick wall cell

protoxylem was rounded by thick wall cell; metaxylem scattered

Protoxylem in peripher; metaxylem scattered

Protoxylem in peripher; metaxylemscattered

Phloem Thick wall, scattered Thick wall, scattered Thick wall, scattered Thick wall, scattered Thick wall, scattered Stele Anomalous Anomalous Anomalous Anomalous Anomalous

Laticifer Distribution Cortex and stele Cortex and stele Cortex and stele Cortex and stele Cortex and stele Type Non anastomosis Non anastomosis Non anastomosis Non anastomosis Non anastomosis

Rhizome Morphology Color White White White White White Surface Soft Soft Soft Soft Soft

Anatomy Epidermis Number 1 layer 1 layer 1 layer 1 layer 1 layer Shape Four sides Four sides Four sides Four sides Four sides

Periphery zone Parenchyma shape Irregular Irregular Irregular Irregular Irregular

Central zone Xylem 1, trachea 1, trachea 1, trachea 1, trachea 1, trachea Phloem One side of xylem One side of xylem One side of xylem One side of xylem One side of xylem Vascular bundle type Close collateral Close collateral Close collateral Close collateral Close collateral Stele Atactostele Atactostele Atactostele Atactostele Atactostele

Pith No pith No pith No pith No pith No pith Articulate latisifer Near phloem scattered scattered scattered Near phloem

cells were near the phloem tissue, and this was supposed to be articulate type. According to Fahn (1990) the articulate laticifer tubes developed in the phloem tissue of stem and contain of tannin.

The differences of anatomical characteristic of rhizome of five banana cultivar were presented in Table 1.

Paradermal section Pseudostem. Actually the pseudostem of banana was

the result of growth and development of the leaf midrib surrounding the rhizome. By peeling the pseudostem it was noted that the structure of epidermis (outer and inner) layer consisted of epidermis cells and stomata.

Epidermis. The shape of outer and inner epidermis cells were rectangular. The arrangement of epidermis cell were compact without inter-cellular space. According to Fahn (1990) the epidermis cells of monocotyledonous stem were stretched lengthwise. The size of inner epidermis cells were

longer and wider than those of the outer one. The longest and widest size of outer epidermis cells

were found in Raja nangka cultivar (AAB genome) with average of 63.756±9.957 µm and 16.936±2.159 µm. The shortest size of outer epidermis cells was found in Kluthuk warangan cultivar (BB genome) which was 40.964±8.684 µm and Penjalin cultivar (AA genome) was 12.936±2.159 µm. The epidermis cells size of triploid cultivar were bigger than that of diploid cultivar. The traits of epidermis layer of three grasses plant had been observed by Sylvester et al. (2001).The trait of leaf epidermis layer in young and adult maize was distinctly, but similar differences were not found in rice and bluegrass leaf.

The longest and the widest size of inner epidermis was found in Kluthuk warangan (BB genome) with average of 71.7764±6.765 µm, and the widest one was Ambon warangan cultivar (AAA genome) with average of 36.344±5.924 µm. The shortest size of Kluthuk susu (ABB


171

1A 1B 2A 2B

Figure 1. Cross section of root of M. paradisiaca cv. A. Kluthuk warangan (BB), B. Klutuk Susu (ABB). a, epidermis; b, cortex; c, endodermis; d, pericycle; e, vessel; f, phloem; g, air space; h, laticifer. Bar = 250 um.

Figure 2. Cross section of rhizome: I. M. acuminata cv. Penjalin (AA) II. M. acuminata cv. Ambon warangan (AAA). Note: A, periphery zone; B, centre zone; 1, epidermis; 2, vessel; 3, phloem; 4, laticifer. Bar = 250 um.

Figure 3. Epidermis layer of pseudostem of five banana cultivars. A. Outer layer; B. Inner layer. 1. M. acuminata cv. Penjalin (AA); 2. M. acuminata cv. Ambon warangan (AAA); 3. M. balbisiana cv. Kluthuk warangan (BB); 4. M. paradisiaca cv. Kluthuk susu (ABB); 5. M. paradisiaca cv. Raja nangka (AAB) e. epidermis cell; st. stoma. Bar = 50 um.

A B Figure 4. Cross section of leaf petiole: A. M. acuminata cv. Penjalin (AA); B. M. acuminata cv Ambon warangan (AAA) a. epidermis; b. parenchyma cells; c. aerenchyma; d. schlerenchyma sheath; e. xylem; f. phloem; g. laticifer; h. air space; i. schlerenchyma; j. cuticle.

st

st

e st

st

st

st

st

st

st st

e

e e e

e

e

e

e

e

A

B


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A B Figure 5. Leaf cross section: A. M. balbisiana cv. Kluthuk warangan (BB); B. M. paradisiacal cv. Kluthuk susu (ABB). a. adaxial epidermis; b. cuticle; c. pallisade tissues; d. spongy tissue; e. xylem; f. phloem; g. schlerenchyma; h. bundle sheath; i. laticifer; j. abaxial epidermis; k. stomata; l. air space. Bar = 500 um. Figure 6. Leaf epidermis of five banana cultivars. A. Adaxial surface; B. Abaxial surface. 1. M. acuminata cv. Penjalin (AA); 2. M. acuminata cv. Ambon warangan (AAA); 3. M. balbisiana cv. Kluthuk warangan (BB); 4. M. paradisiaca cv. Kluthuk susu (ABB); 5. M. paradisiaca cv. Raja nangka (AAB). e. epidermis cell; st. stoma. Bar =50 um.

genome) with average of 53.9±5.553 µm, while the narrowest one was Kluthuk warangan’s (BB genome) with average of 28.336±2.798 µm. It was showed from the result that the size of epidermis layer did not depend on the ploidy level. Statistical analyzis showed that ploidy level had significantly affect on outer epidermis cell size of pseudostem. Suryo (2007) supposed that the higher level of ploidy, the bigger epidermis cells.

Stomata. Stomata were located on inner and outer parts of pseudostem epidermis layer. The guard cell of stomata were kidney like, rounded by 4-6 subsidiary cells. This condition was in line with Fahn (1990) statement, that the Musaceae family had 4-6 subsidiary cells. The structure of the the subsidiary cell was quite similar to the epidermis cell around them, so the type of this stomata was called anomositic.

The stomata of Penjalin and Kluthuk susu cultivar were surrounded by 4-7 cells and 4-8 cells respectively. The distribution and the shape of stomata either in outer or inner epidermis layer were different. Statitical analysis showed that the ploidy level significantly affected to the length of the stomta in outer epidermis layer. Penjalin (AA genome) and Kluthuk warangan (BB genome) cultivar

showed no differences length of stomata in outer epidermis (i.e. 26.488±1.288 µm and 26.488±2.962 µm). In triploid level group of banana, the length of stomata also showed no significantly different. The average of stomata length of Ambon warangan cultivar was of 33.572±2.284 µm, the average of Kluthuk susu cultivar’s was 33.418±0.689 µm, and the average of Raja nangka cultivar’s was 32.956±2.066 µm.

The highest number of stomata (mm-2) in outer epidermis was found in Penjalin cultivar (AA genome): 14.55±7.476, with stomata index of 1.55%, while the lowest number was found in Kluthuk warangan (BB genome). The higest number of stomata in inner epidermis was found in Kluthuk warangan cultivar, and the lowest was found in Raja nangka. The density of stomata in outer epidermis layer was higher than that in inner epidermis layer. This condition was supposed to be related to the function of stomata. In outer epidermis layer, stomata were directly connected with atmosphere to catch oxygen, to facilitate their function as respiration, transpiration and photosynthesis processes. The anatomical characters of pseudostem of five cultivars were presented in Table 2 and Figure 3.

A

B

st

e

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ee

e

e

e

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st st


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Table 2. The stomata characters of pseudostem and leaf in five banana cultivars (AA, BB, AAA, ABB, AAB) of different ploidy levels.

Character Cultivar

Penjalin (AA) Kluthuk warangan(BB)

Ambon warangan (AAA)

Kluthuk susu (ABB)

Raja nangka (AAB)

Characters of pseudostem stomata Outer stomata Subsidiary cell 4 -7 4-6 4-6 4-8 4-6 Length (μm) 26.488±1.288a 26.488±2.962a 33.572±2.284b 33.418±0.689b 32.956±2.066b

Width (μm) 26.488±2.755a 34.804±2.066b 31.416±4.016b 42.50±2.335c 41.58±4.747c

Number of stomata (per 1 mm²) 14.55±7.476b 7.28±4.07a 10.01±2.035ab 9.1±3.217ab 8.19±3.807ab

Number of epidermis (per 1 mm²) 924.56±75.89b 1188.46±16.841d 1090.18±0.133c 987.35±100.636b 839.02±46.133a

Stomata index 1.55% 0.61% 0.91% 0.91% 0.97%Inner stomata Subsidiary cell 4-6 4-5 4-6 4-5 4-5 Length (μm) 27.412±2.284ab 31.724±1.377bc 35.42±3.772c 28.644±5.51ab 25.872±2.008a

Width(μm) 24.948±5.803a 44.968±4.671b 37.884±4.016b 38.192±5.04b 25.872±6.748a

Number of stomata (per 1 mm²) 7.28±4.07ab 8.19±2.035b 7.28±2.492ab 5.46±2.035ab 3.64±2.035a

Number of epidermis cells (per 1 mm²) 483.21±62.17d 308.58±37.877b 403.13±31.947c 322.14±8.139b 223.95±18.482a

Stomata index 1.48% 2.59% 1.77% 1.67% 1.61%

Character of leaf stomata Stomata of adaxial epidermis Number of subsidiary cell 4-6 4 4-5 4 4-5 Length (μm) 27.412±1.687a 26.488±2.530a 33.88±1.089b 32.032±1.756b 35.112±2.008b

Width (μm) 28.028±1.756a 27.412±2.755a 30.492±1.687ab 34.804±2.577c 32.956±1.377bc

Number of epidermis (per 1 mm²) 1716.26±139.144b 1509.69±293.209b 2063.88±180.933c 1708.98±297.436b 975.52±104.778a

Number of stomata (per 1 mm²) 49.14±4.984d 13.65±4.55a 37.31±9.864c 16.38±7.614ab 22.75±3.217b

Stomata index 2.78% 0.90% 1.78% 0.95% 2.28%Stomata of abaxial epidermis Number of subsidiary cell 4 4 4 4 4 Length (μm) 23.1±1,54a 24.024±1.756ab 29.568±1.288c 26.796±2.577bc 24.948±3.339ab

Width (μm) 27.104±3.002bc 30.184±1.756c 24.024±1.756b 24.332±2.284b 19.866±3.285a

Epidermis number (per 1mm²) 1076.53±108.658c 594.23±72.771ab 1138.41±112.072c 515.06±76.434a 715.26±101.302b

Stomata number (per 1 mm²) 141.05±12.461b 192.01±18.870c 125.58±6.900a 190.19±3.807c 125.58±4.07a

Stomata Index 11.58% 24.42% 9.94% 26.97% 14.94%Note: values followed by different rates in the same column are not significantly different in DMRT with α = 5%.

Morphology and anatomy of leaf Morphology

The leaf of banana belongs to the complete type, because they have midrib, stalk (petiole) and blade (lamina). In banana, modification of midrib was called pseudostem, surrounding the true stem. In cross section the shape of petiole was look-like half circle and the dorsal side was shallow grooved or deep grooved. The side part of Penjalin (AA genome) petiole and Ambon warangan (AAA genome) cultivar broaded and look-like wing. Two other cultivars (BB and ABB genome) petiole their side part were close, while Raja nangka cultivar (AAB genome) as hybrid from natural crossing between M. acuminata (AA genome) and M. balbisiana (BB) the side part of petiole was open upright. According to Jumari (2007) AAB genome was originated from two set genome of M. acuminata (AA) and one set genome of M. balbisiana (BB). The shape of the five cultivars leaves is oblonge with flat tip and entire margin. The ratio of the length and the wide of M. paradisiaca leaf was (2.5 -5): 1. According to Nugroho et al. (2003), this condition was oblonge type.

Anatomy Petiole compossed of three tissue systems i.e.:

epidermis layer, ground tissue system (parenchyma tissue) and vascular system. Morphological and anatomical

examination of the petioles and leaves of Musa textilis suggested how these two apparently incompatible abilities are achieved. The hollow U‐shaped section of the petiole and the longitudinal strengthening elements in its outer skin give it adequate rigidity, while its ventral curvature help support the leaf without the need for thick lateral veins. These features, however, also allow the petiole to reconfigure by twisting away from the wind, while the leaf can fold away. In addition, two sets of internal structures, longitudinal partitions and transverse stellate parenchyma plates, help prevent dorsoventral flattening, allowing the petiole to flex further away from the wind without buckling (Ennos et al. 2000).

Epidermis layer compossed of a single layer, with compact cell, rectangular shape and was protected by cuticule. The position of parenchyma cells was irregular. In the middle part of the petiole, there were big air space and the parenchyma cells filled with air. The shape of air parenchyma cells was star-like, and formed network to each other. Many crystal needle-like and laticifer were distributed between those cells. In Rustia formosa (Rubiaceae), both the adaxial and abaxial epidermis are compossed of polygonal cells.The epidermis cell in maize leaf were uniformly. The juvenile adaxial leaf of maize were covered with epicuticular wax, lack of hair and bulliform cell, whereas the adult leaf is pubescent with


174

bulliform cells but lack epicuticular waxes. In contrast, the adaxial epidermis in rice and bluegrasses leaf were covered with both epicuticular waxes and hairs (Sylvester et al. 2001).

Vascular bundles in petiole consisted of two groups, first group small located beneath the epidermis layer row regularly, while the big one distributed irregularly in the inner side. The type of vascular bundle was close collateral, consisted of xylem and phloem elements, and both were surrounded by thick wall (schlerenchyma). In big vascular bundle, the xylem consisted of vessel and tracheid, while the small one consisted of vessel only. The position of xylem in petiole was in upper side while phloem in lower side. Anatomy of petiole presented in Figure 4.

Blade (lamina). The blade consisted of epidermis layer, vascular bundles and parenchyma cells. The shape of epidermis cells was rectangular. The longest epidermis size was found in Penjalin cultivar, the widest was found in Kluthuk susu cultivar, the shortest was found in Raja nangka cultivar, and the narrowest one was found in Kluthuk warangan. The size of adaxial epidermis was bigger than that of abaxial epidermis. In Penjalin and Kluthuk susu cultivars hypodermis layer was found beneath the upper epidermis layer, whereas Kluthuk susu cultivar had two layers of hypodermis. Hypodermis were not found in the other three banana cultivars. According to Vieira et al. (2001) research, both the adaxial and abaxial epidermis of. R. formosa are composed of polygonal cells. Similar with the Kluthuk susu cultivar, the adaxial epidermis of this spesies were composed of two layer of cells, while the abaxial one was a single layer.

The abaxial epidermis of banana leaf were covered with cuticle. Trichome (hair) was not found in epidermis layer of banana. Epidermis, hair layer and cuticle as protective tissues that first intercept radiation. This tissues protecting the leaves against ultraviolet-B radiation (Karabourniotis et al. 1998).

Mesophyll (tissue between adaxial and abaxial epidermis) consisted of pallisaden and spongy tissues. These tissues consist of chloroplast which contain chlorophyll pigment. There were two pallisaden layers were found and has dense arrangement. Some of spongy cells breakdown and formed big airspace. Some of spongy cells filled with few chloroplast. This condition is the general structure of banana leaf (Tomlinson 1969). The size of airspace and the thick of mesophyll of five cultivars showed different one to the other.

Similar with banana, mesophyll of R. formosa also compossed of two palisade and several layer of spongy parenchyma, but no airspace were found (Vieira et al. 2001).The typical of both leaf based on the mesophyll composition was dorsiventral. Spongy parenchyma consist of thin-walled cell, and irregularly placed.The airspace in spongy layer may be lysigenous or schizogenous origin. Research of Turner (1999) and Turner et al.(1998) showed that most cavities and canals in leaf mesophyll thought to be lysigenous and schizogenous origin. Turner et al. (1998) presented evidence that lysigenous appearance in Citrus lemon, and schizogenous origin was found in R. formosa (Vieira et al. 2001)

Vascular tissues distributed in mesophyll, consisted of small and big. The big vascular bundle compossed of vessel, tracheid, fiber, parenchyma cells and phloem (Tomlinson 1969). The vascular bundle of the five cultivars is compossed of xylem and phloem elements. The bundle surrounded by the parenchymatic or sclerenchymatic cells, was called bundle sheath. The small bundles were not protected by bundle sheath. Laticifer were scattered between pallisaden cells or in spongy tissue near the abaxial epidermis. Raja nangka cultivar produced fewest laticifer. The anatomy character of leaf blade can be seen Figure 5.

Stomata. Stomata were found on both surface of epidermis layer. The type of stomata was panerophor because the potition of guard cell in line with epidermis layer. This result was supposed by Tomlinson’s research (1969). The shape of guard cell was kidney-like. Each stoma was surrounded by 4-6 cells. The distribution, the size and the index of stomata were varied in five banana cultivars. The size of triploid stomata on the upper and lower epidermis layer of leaves longer than the diploid one. The ploidy level affects this character significantly to the lenght and the width of stomata in upper epidermis layer. The lenght of stomata in diploid cultivars have no significantly different, as well as in triploid cultivars. In abaxial epidermis of Kluthuk warangan distribution of stomata was higer than the others (192.01±18.87) (see Table 2.).The number of subsidiary cells was four to six cells. The number of subsidiary cells in R. formosa three to six with various shape (Vieira et al. 2001). Stomata present only in the abaxial surface with the calculated average number of 133 stomata/mm2. The type of stomata was predominantly paracytic. The size and distribution of banana stomata were presented in Table 2.

CONCLUSION

Stem and leaf morphology character of diploid level (AA and BB genome) was different from triploid level (AAA, AAB, and ABB genome). Anatomy and morphology character of root and rhizome of banana in diploid level and triploid level was quite similar. Distribution of stomata was found in leaf and pseudostem. Stomata was found in adaxial and abaxial epidermis layer. The size of guard cells in triploid cultivars is longer than that diploid vultivars. The root composse of epidermis layer, cortex and cylinder vascular of five cultivar’s root show anomalous structure. Rhizome consist of peripheric and centre zone. Anatomically, there was no differences in the rizome structur between five banana cultivars. The row of vascular bundles act as demarcation area between peripheric and central zone. In cultivar with BB genome (diploid) and ABB genome (triploid) the row of vascular bundle was not found. The differences of leaf anatomy are base on: size and number of stomata distribution, number of subsidiary cells, number of hypodermal layer, structure and mumber of parenchyma palisaden, size of airspace in petiole and mesophyll and the vascular bundle structure.


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ACKNOWLEDGEMENTS

Thank full to Utaminingsih who has helped preparing this manuscript; and Prof. Dr. Sumardi M.For.Sc. for editing this manuscript.

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Marine Actinomycetes screening of Banten West Coast and their antibiotics purification

ROFIQ SUNARYANTO♥, BAMBANG MARWOTO Center of Biotechnology BPPT, PUSPIPTEK, Serpong, Tangerang Selatan 15340, Banten, Indonesia Tel./Fax.+62 21 7560208, ♥email:

[email protected]

Manuscript received: 18 May 2010. Revision accepted: 2 November 2010.

ABSTRACT

Sunaryanto R, Marwoto B (2010) Marine Actinomycetes screening of Banten West Coast and their antibiotics purification. Biodiversitas 11: 176-181. Isolation and purification of active compounds produced by marine Actinomycetes has been carried out. Marine sediment samples were obtained from six different places at Anyer, Banten West Coast in October 20, 2007. Isolation was carried out using two methods pretreatments, acid treatment and heat shock treatment. A total of 29 Actinomycetes isolates were obtained from the various sediment samples collected, then tested for antimicrobial test against Escherichia coli ATCC 25922, Staphylococcus aureus ATCC25923, Pseudomonas aeruginosa ATCC27853, Bacillus subtilis ATCC 66923, Candida albicans BIOMCC00122 and Aspergillus niger BIOMCC00134. Identification of potential isolate was carried out using 16S rRNA. Purification of active compound was carried out using silica gel column chromatography and preparative HPLC. Result of this research showed that isolate A11 produced the most active compound against Gram-positive and Gram-negative bacteria. Morphology and identification test using 16S rRNA gen showed that isolate A11 is Streptomyces sp. Production of active compound from isolate A11 used yeast peptone medium. The single peak of active compound was detected by HPLC and showed retention time on 8.35 min and maximum absorbance UV visible of antibiotic was 210 nm and 274.5 nm. Active purified compound showed inhibition activity to Gram-positive and Gram-negative bacteria. Minimum inhibitory concentration (MIC) to E. coli ATCC 25922 was 27 µg/mL, P. aeruginosa ATCC 27853 68.7 µg/mL, S. aureus ATCC 25923 80.2 µg/mL, and B. subtilis ATCC 66923 73.7 µg/mL.

Key words: marine Actinomycetes, isolation, screening, antimicrobial activity, minimum inhibitory concentration.

INTRODUCTION

Actinomycetes are the most widely distributed group of microorganisms in nature which primarily inhabit the soil (Goodfellow et al.1983; Locci et al.1983). Almost 70% of the world antibiotics are known to come from Actinomycetes, mostly from the genera Streptomyces and Micromonospora (Berdy 2005; Goodfellow et al.1988). Previously, researchers are more focused on explore at terrestrial Actinomycetes. Nowdays, new antibiotics has been found from marine Actinomycetes (Fiedler et al. 2005; Ghanem et al. 2000; Lam 2006).

Although the exploitation of marine Actinomycetes as a source for discovery of novel secondary metabolites is at early stage, numerous novel metabolites have been isolated in past few years. As example, abyssomicin C is novel polycyclic polyketide antibiotic produced by a marine Verrucosispora strain (Riegdlinger et al. 2004). Abyssomicin C possesses potent activity against Gram-positive bacteria, including clinical isolates of multiple-resistant. Diazepinomicin is a unique farnesylated dibenzodiazepinone produced by a Micromonospora strain (Charan et al. 2004). It possesses antibacterial, anti-inflammatory and antitumor activity. Salinosporamide A is a novel βlactone-γ-lactam isolated from fermentation broth

of a new obligate marine Actinomycete, Salinispora tropical (Feling et al. 2003).

Indonesia is archipelago country that has wide sea area, that is more than 3.1 million km2. The high characteristic of sea showed a high of biodiversity such as microorganism, plant, and animal. Nevertheless this potency has been not exploited. Currently exploration of Actinomycetes in Indonesia still limited to terrestrial Actinomycetes. The objective of this research are isolation and purification active compound which produced by marine Actinomycetes (isolate A11).

MATERIALS AND METHODS

Sample collection and processing Sediments were obtained from six locations of marine

site in Anyer, Banten West Coast in October 20, 2007. From each location, six sediment samples of 5 g each were collected from 10 to 15 cm below the surface. Each of the sediment samples for each site was placed in small pre-labeled plastic bags which were tightly sealed. Serial dilutions up to 10- 6 were then prepared for each of the six samples. Hereinafter each sample is given code in accordance sampling location.

SUNARYANTO & MARWOTO – Antibiotics of marine Actinomycetes

177

Isolation of Actinomycetes All sediment samples were processed in laboratory as

soon as possible after collection. The samples were suspended in sterilized water and were made serial dilution. Pretreatment were conducted using acid and heat-shock treatments. Acid treatment was conducted by the acidifying the samples to pH 2 were obtained for 3 hours. Heat-shock treatment was conducted by the heating the samples at 60ο C for 4 hours (Pisano et al. 1986). Treated samples were then inoculated onto starch agar medium (1% w/v starch, 0.4% w/v yeast extract, 0.2% w/v peptone, natural seawater and 2% w/v agar) and incubated for 4-8 weeks at room temperature. One hundred gram per milliliter of nalidixic acid and 5 g/mL of rifampicin were added to reduce the number of unicellular bacteria (Pisano et al. 1989). The antifungal agent cycloheximide (100 g/mL) and 25 g/mL nystatin were added to all isolation media. Actinomycetes colonies were recognized by the presence of branching, vegetative filaments and the formation of tough, leathery colonies that adhered to the agar surface. Morphologically diverse Actinomycetes were repeatedly transferred to the same media until pure cultures were obtained. All pure strains were grown in yeast extract-malt extract (YEME) broth and cryopreserved at -80° C in 10% v/v glycerol solution.

Actinomycetes identification based on 16S rRNA analysis.

DNA isolation. The DNA was isolated using FastPrep kit for DNA isolation. The pellet was lysised using lysing matrix, added with 1000 µL and homogenized using FastPrep instrument for 40 second at 4500 rpm.

DNA amplification and purification. PCR was done for DNA amplification using 8F and 1492R primers. The PCR mixture containing 8F and 1492R primers was added to the DNA solution. The PCR product was then purified using Gel/DNA extraction kit.

16S rRNA gene sequencing. The 16S rRNA gene obtained was submitted to the DNA sequencing facility, Genetic laboratory, Biotech Centre. A big Dye® terminator V 3.1 cycle sequencing kit was used to sequence the DNA. The DNA was then run in an automated DNA sequencer using capillary electrophoresis system, ABI 300 genetic analyzer. The sequence was compared to a database available at NCBI using BLAST search.

Liquid culture of active substance A well grown agar slant of isolate was inoculated into a

250 mL flask containing 100 mL of the vegetative medium (YEME medium) consisting of: bacto peptone 5 g/L, yeast extract 3 g/L, malt extract 3 g/L, glucose 3 g/L, demineral water 250 mL, and sea water 750 mL. pH value of the medium was adjusted at 7.6 before sterilization. The flask was incubated at 30º C for 2 days in incubator shaker. Fifty milliliter of this culture was transferred to 1000 milliliter of the fermentative medium (Nedialkova et al. 2005). Fermentative medium consisting of bacto peptone 15 g/L, yeast extract 3 g/L, Fe(III) citrate hydrate 0.3 g/L, demineral water 250 mL, and sea water 750 mL. pH value of the medium was adjusted at 7.6 before sterilization. The

fermentation was carried out at 30ºC for 5 days in incubator shaker (Kanoh et al. 2005).

Extraction and purification The culture broth was centrifuged at 14000 x g for 15

min. The dark filtrate was divided and extracted using ethyl acetate solvent. Filtrate and organic solvent was mixed thoroughly by shaking them in 1000 mL capacity separating funnel and allowed to stand for 30 min. Two layers were separated; the aqueous layer and the organic layer, which contained the solvent and the antimicrobial agent. The organic layer was concentrated by evaporation under vacuum to the least volume, after the dehydration with anhydrous Na2SO4. The aqueous layer re-extracted and the organic layer added to the above organic layer. The organic layer was concentrated by evaporation under vacuum again.

Dry extract of supernatant and biomass were purified using column chromatography. Dry extract was injected on column chromatography then eluted stepwise with chloroform-methanol solvent system as follows: First the column was eluted with 100% chloroform (Fraction 1). This repeated by reducing the chloroform by 10% in each fraction and the methanol was increased by 10% in each fraction until percentage of methanol 100%. Thirty fraction were collected (each of 20 mL) and tested for their antimicrobial activities. Then the active fractions obtained from column chromatography were further purified by preparative HPLC.

Preparative HPLC Purification by preparative HPLC was conducted using

a Waters 2695 HPLC, photodiode array detector (PDA), and Column puresil 5μ C18 4.6x150 mm. The volume injected was 100 µL per injection under conditions of average pressure of 1.267 psi, and the flow rate was 1 mL/min where the mobile phase was 0-45% methanol–water and time period was 25 min (Kazakevich and Lobrutto 2007).

Antimicrobial activity assay Antimicrobial activity was monitored by the agar

diffusion paper-disc (6 mm), which are dripped by extract solution, dried and then placed over the agar surface plates freshly inoculated with the Escherichia coli ATCC 25922, Staphylococcus aureus ATCC25923, Bacillus subtilis ATCC 66923, Pseudomonas aeruginosa ATCC27853, Candida albicans BIOMCC00122 and Aspergillus niger BIOMCC00134 as test organism. Suspensions of test organisms were adjusted to 106 cfu/mL. The most potent isolates were noted for each test microorganism, based on the mean diameter of inhibition zones.

Analysis HPLC HPLC analysis was performed using an analytical

column Sunfire (4.6 x 250 mm, Shiseido Co. Ltd., Tokyo, Japan), elution using methanol-water (0-100% linear gradient for 25 min and then isocratic elution with 100% methanol until 10 min), at a flow rate of 1 mL/min and detection at 210 nm.


178

Determination of the minimum inhibitory concentration (MIC)

MIC determinations were performed using the agar-dilution methods according to modified methods of Bonev et al. (2008) and Andrews (2001). Active purified compound was dissolved in methanol (6500 μg/mL concentration) were taken as standard stock. A series of two fold dilutions of each extract in the final concentration of 25 μg/mL were dripped on paper disc 6mm, dried and then placed over the agar surface plates freshly inoculated with either E. coli ATCC 25922, S. aureus ATCC25923, B. subtilis ATCC 66923, and P. aeruginosa ATCC27853 as test organisms. The value of logarithm of MIC (Log MIC ) was determined as the zero intercept of a linear regression of logarithm of concentration Log[C] as Y axis versus the squared size of clear zones diameter (X2) as X axis. MIC is antilogarithm the intercept.

RESULTS AND DISCUSSION

Isolation and screening of Actinomycetes from marine The five sediment samples of the sampling area yielded

29 Actinomycetes isolates. Eight of the 29 Actinomycetes isolates showed antimicrobial activity, 2 isolates active against E. coli ATCC 25922, 4 isolates active against S. aureus ATCC25923, 2 isolates active against B. subtilis ATCC 66923, 3 isolates active against P. aeruginosa ATCC27853, 3 isolates active against C. albicans, and 2 isolates active against A. niger (Table 1).

Some of sediment samples obtained many isolate of Actinomycetes, but some of them did not contain Actinomycetes. It indicates that Actinomycetes are distributed unevenly in Banten, West Java Coast. When compared with brackish Actinomycetes, the population of marine Actinomycetes was less. Actinomycetes are less common in marine sediments relative to brackish environments (Goodfellow and Williams 1983; Parungao et al. 2007). Another study (Goodfellow and Haynes 1984) suggested that Actinomycetes represent only a small component of the total bacterial population in marine sediments. They observed that most of the isolates were of terrestrial and brackish origin. Terrestrial soils have been the main reservoir of Actinomycetes. They comprise a large part of the microbial population of the soil (Parungao et al. 2007). Table 1 shows that many Actinomycetes had antibacterial activity rather than anti fungal activity, same as reported by Berdy (2005). In the group of antibiotics, 66% are antibacterial (Gram-positive and Gram-negative), and 34% are anti fungi including yeast.

From eight isolates which active against bacteria test, only one was chosen to next study. A11 isolate showed high activity against Gram-positive and Gram-negative bacteria. A11 isolate was selected for next study. From identification using 16S rRNA was obtained the information that isolate A11 was Streptomyces sp., homology 100% to Streptomyces sp. J22, class Actinobacteria, order Actinomycetales, family Streptomycetaceae, and genus Streptomyces. Morphology of A11 is the same like genus of Streptomyces (Chater

2006; Antonova-Nikolova et al. 2007). Surface looked glossy and circular with folding hyphae that length and formed some antenna (aerial hyphae) arising out in vertical were characteristic of Streptomyces morphology (Flardh and Buttner 2009). Streptomyces are the one a genus of Actinomycetes that morphologically resemble fungi and physiologically resemble bacteria. Subsequent growth of Streptomyces colonies as they spread over the agar surface is thought to follow similar kinetics to filamentous fungi (Bushell 1988). The colony growth of the Streptomyces is initiated when a spore germinates, giving rise to one or more long multinucleoid filaments. These filaments elongate and branch repeatedly, originating a vegetative mycelium (substrate mycelium) that develops over, and into the culture medium (Miguelez et al. 1999).

Table 1. Eight isolates of Actinomycetes (Banten West Java Coast) producing antimicrobial active compound.

Name of isolate

Sample pre-treatment

Antimicrobial (clear zone diameter in mm)

E.co

li

S.ae

reus

B.su

btili

s

P.ae

rugi

nosa

C.al

bica

n

A.ni

ger

A61 HS 0 0 0 0 0 0 A62 HS 0 0 0 0 0 0 A63 HS 0 0 0 0 0 0 A64 HS 0 0 0 0 0 15 A65 HS 0 0 0 0 0 0 A66 HS 0 0 0 0 0 0 A67 A 0 0 0 0 0 0 A68 A 0 0 0 0 0 0 A69 A 0 0 0 0 0 0

A610 A 0 12 0 0 0 0 A611 A 0 0 0 0 0 0 A11 HS 18 15 14 14 0 0 A12 HS 0 0 0 0 0 0 A21 HS 0 0 0 7 0 9 A23 A 0 0 0 0 0 0 A24 A 0 0 0 0 0 0 A31 HS 0 0 0 0 0 0 A32 HS 0 12 0 0 7 0 A33 HS 0 0 0 0 0 0 A41 HS 0 0 0 0 0 0 A42 HS 0 0 0 0 0 0 A43 A 10.16 0 8.67 9.51 0 0 A44 A 0 0 0 0 10.61 0 A45 A 0 0 0 0 0 0 A51 HS 0 0 0 0 0 0 A52 HS 0 0 0 0 0 0 A53 HS 0 0 0 0 0 0 A54 HS 0 8.56 0 0 8.67 0 A56 A 0 0 0 0 0 0

Note: HS : Heatshock treatment, A: Acid treatmeant, Diameter of paper disc: 6 mm.

The phylogenic tree (Figure 1) indicated that A11 has

close contiguity with S. tanashiensis subsp. cephalomyceticus. An isolate of S. tanashiensis subsp. cephalomyceticus was recognized which could synthesize TAK-637 (tachykinin-receptor-antagonist) (Tarui 2001).


179

Figure 1. Polygenetic tree of isolate A11 shown as Streptomyces sp. Fermentation and purification

Fermentation of isolate A11 was carried out for 7 days with yeast-peptone medium. At the last day of fermentation, the medium color became dark and more viscous than first day. It was looked many white granular in the bottom of flask. From 5 liters volume of fermentation was obtained 4.72 g of dry biomass after extracted by methanol, and methanol extract of biomass was obtained 2.72 g, extract of supernatant was obtained 0.33 g. Antimicrobial bioassay

A11

Streptomyces parastreptomyces abscessus

Streptomyces streptoallomorpha polyantibiotica

Streptomyces microflavus strain HBUM174133

Streptomyces africanus

Streptomyces microflavus

Streptomyces paresii

Streptomyces afghaniensis

Streptomyces roseoviolaceus

Streptomyces kitasatospora

Streptomyces streptacidiphilus

Streptomyces sp LS247

Nocardioides thermolilacinus

Streptomyces malaysiensis

Nocardia abscessus

Streptomyces sp. QM-B814 Candidatus streptomyces philanthi biovar

Streptomyces indonesiensis

Streptomyces brasiliensis

17

57

31

7

5

100

45

100

99

4

2

51

39

18

8

19

24

2

Streptomyces tanashiensis subsp. cephalomyceticus

Actinomadura

Table 2. Biological activity of biomass and supernatant extract from isolate A11

Sample Diameter of inhibition/clear zone (mm) S. aureus B. subtilis P. aeruginosa E. coli C. albicans A. niger

Biomass extract - - - - - - Supernatant extract 10.39 24.43 9.64 9.55 - - Positive control (rifampicin 500 ppm)

21.27 44.57 10.08 10.12 - -

Note: Diameter of paper disc: 6 mm.

Table 3. Minimum inhibitory concentration (MIC) of active purified compound.

Sample Minimum Inhibitory Concentration (MIC) µg/mL E. coli

ATCC 25922 S. aureus

ATCC 25923 B. subtilis

ATCC 66923 P. aeruginosa ATCC 27853

Active purified compound 27 80.2 73.7 68.7 Tetracycline (positive control) 64.0 256 128 12.5


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showed that extract of supernatant active to bacterial test, but extract of biomass have no activity to bacterial test. The data of biological activity extract fermentation from isolate A11 is presented in Table 2. Table 2 showed that there were strong antibacterial activities on supernatant extract, but no in the biomass extract. This indicates that isolate A11 produced antibacterial substance by extracellular secretion.

Further purification of the antibiotic has been carried out using column chromatography and preparative HPLC. Antibacterial test to all fraction of preparative HPLC showed that peak retention 10.1 min was active fraction. Active fraction was collected and test to analysis HPLC. Analysis HPLC chromatogram of active fraction and UV visible spectrum was presented at Figures 2 and 3.

Figure 2 showed that active fraction of antibiotic has retention time 8.6 min at gradient elution methanol-water 0-100% using column sunfire. Purification using preparative HPLC obtained single peak with maximum absorbance UV visible was 210 nm and 274.5 (Figure 3). This compound indicated that was colorless or white powder.

AU

0.00

1.00

2.00

3.00

Minutes0.00 5.00 10.00 15.00 20.00 25.00 30.00 35.00

8.62

3

Figure 2. Analysis HPLC chromatogram of active fraction

AU

0.00

0.20

0.40

0.60

0.80

1.00

1.20

1.40

nm250.00 300.00 350.00

274.5

Figure 3. UV visible spectrum of active fraction.

Isolate A11 was chosen to be subjected for minimum inhibitory concentration (MIC) assay since it exhibited the larger zone of inhibition. Table 3 showed that active compounds produced by isolate A11 was highly active against E. coli ATCC 25922, S. aureus ATCC25923, P. aeruginosa ATCC27853, B. subtilis ATCC 66923, with respective MIC value 27, 80.2, 68.7, and 73.7 µg/mL. This indicating that this active compounds highly active against Gram-positive and Gram-negative bacteria. It was

compared tetracycline, this active compound was stronger active against E. coli ATCC, S. aureus ATCC25923, and B. subtilis ATCC 66923, but rather weaken against P. aeruginosa ATCC27853.

CONCLUSION

Actinomycetes (isolate A11) was isolated from sedimen in Anyer, Bnaten produced antibiotic active against to Escherichia coli ATCC 25922, Staphylococcus aureus ATCC25923, Pseudomonas aeruginosa ATCC27853, Bacillus subtilis ATCC 66923. Identification using 16S rRNA showed that isolate A11 is Streptomyces sp. Purification of antibiotic using column chromatography and preparative HPLC produce single peak of chromatogram at retention time 8.623 min and max UV absorbance was 210 nm and 274.5 nm. Minimum inhibitory concentration (MIC) to E. coliATCC 25922 was 27 µg/mL, P. aeruginosa ATCC 27853 68.7 µg/mL, S. aureus ATCC 25923 80.2 µg/mL, and B. subtilis ATCC 66923 73.7 µg/mL.

ACKNOWLEDGMENTS

We thank to Anis Mahsunah (Head of Downstream Processing Laboratory) and Hardaning Pranamuda (Head of Industrial Biotechnology Division, Biotech Center BPPT, South Tangerang) for their valuable and critical comments on this research. We also thanks to IDB (Islamic Development Bank) for supporting scholarship of our study.

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evidence for the existence of a process of cell deletion in a multicellular prokaryote. J Cell Biol 145:515-525.

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Plant diversity in natural forest of Guilan Rural Heritage Museum in Iran

ROYA ABEDI1, HASSAN POURBABAEI2,♥ Department of Forestry, Faculty of Natural Resources, Somehsara, University of Guilan, Islamic Republic of Iran. P.O. Box 1144, Tel.: +98-182-

3220895, Fax.: +98-182-3223600, email: [email protected], 2,♥[email protected]

Manuscript received: 31 August 2010. Revision accepted: 29 October 2010.

ABSTRACT

Abedi R, Pourbabaei H (2010) Plant diversity in natural forest of Guilan Rural Heritage Museum in Iran. Biodiversitas 11: 182-186. The aim of this study was to determine plant species diversity in Guilan Rural Heritage Museum in Iran. Eighty nine sampling plots were sampled based on systematic random method. Data analysis was carried out using diversity indices of Richness, diversity (Shannon-Wiener, Simpson, Mc Arthur’s (N1) and Hill’s (N2) and Smith and Wilson’s evenness index (Evar). Results indicated that Rosaceae and Labiatae families have the highest number of species. Quercus castaneifolia and Ruscus hyrcanus were the most dominant woody plants for class of tree and shrub, respectively. Carex divolsa and Viola odorata were dominant herbaceous species. Herbaceous layer had the highest richness, evenness and diversity. Mc Arthur’s N1 index had the highest value among diversity indices.

Key words: diversity, richness, evenness, Rural Heritage Museum, Guilan.

INTRODUCTION

Deforestation is one of the primary causes of biodiversity loss. Forests represent about 30% of terrestrial habitats, and support an exceptional number of species. Forests also provide economically important products and services. Small, isolated forest fragments are typically less able to provide these goods and services, or support a full complement of native species (Mayer and Tikka 2006). Natural forests decline in both extent and quality worldwide; there is an increasing recognition of the biodiversity conservation value of production landscapes (Le Brocque et al. 2009). Maintenance of biodiversity has been recognized as an important component of sustainable development and protection of native forests is a major means of biodiversity conservation (Muller et al. 2006). Efficiency of management and maintain of endangered species of a region could be evaluated when we have entire consciousness about biodiversity (Asri 2008).

Plant biodiversity consists of diversity into plant population structure, distribution, composition and abundance patterns. It is used as an index for comparison of forest ecosystems conditions (Pourbabaie 2001). Biological diversity has an indispensable value to society in that it (i) serves as a reservoir of genetic material that enhance productivity and stress tolerance of domesticated species and a source of new medicine, energy and industrial feed stock, (ii) provides ecological services such as amelioration of climate, water purification, soil stabilization and flood control and (iii) provides animals and natural landscape which have an overall benefit on human health and well-being through various forms of outdoor recreation (Brockway 1998).

Biological diversity is the richness and evenness of species amongst and within living organisms and ecological complexes (Polyakov et al. 2008). Biodiversity is mostly studied in species level. There are different indices to measure biodiversity. The most commonly considered facet of biodiversity is species richness. Evenness is another important factor of biodiversity. (Kharkwal et al. 2004). Evenness has been considered as a fundamental fact in habitats with more than one species (Hashemi 2010). Nowadays, numerous efforts to incorporate biodiversity into forests management and planning are encouraging (Brockway 1998).

Many studies have been carried out on plant biodiversity indices in Iran and around the world. Gholami et al. (2007) compared plant diversity, richness and evenness indices around protected area of the Bazangan Lake in Khorasan province, northeast of Iran. They indicated the highest value in Shannon-Wiener index. Ravanbakhsh et al. (2007) studied under-storey and over-storey plant biodiversity in Gisoom reserved forest in Guilan province, north of Iran and they showed that under-storey vegetation was disturbed and affected by human impacts. Abasi et al. (2009) investigated the effects of conservation on woody species diversity in protected regions of Oshtorankooh in Lorestan province, west of Iran. They expressed that trees and shrubs living in the protected regions species have significantly higher diversity, richness, evenness and better living condition than they living in non-protected region. Comparison of species richness and Hill’s diversity indices showed that total species richness was higher in natural stands. Also, more fertile sites have significantly higher values of Hill’s diversity index in mature stands of spruce plantation and natural stands in Southeaster New Brunswick, Canada

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(Roberts 2002). Measurement of Shannon-Wiener and evenness indices on Pinus massoniana communities in Conservation project of plant biodiversity in Yangtze Three Gorges reservoir area, China showed that biodiversity of shrubs layer was the highest, followed by grass layer and the middle, while tree layer was the lowest (Tian et al. 2007).

Main objective of this study was to quantitatively analyse the biodiversity of vegetation cover in tree, shrub, herbaceous and regeneration layers in Guilan Rural Heritage Museum, Iran.


Study area The study was carried out at the Guilan Rural Heritage

Museum with approximately 260 ha in extent that is located in Saravan Forest Park in the north of Iran (37˚6΄ to 37˚8΄ N latitude and 49˚37΄ to 49˚39΄ E longitude). The altitude ranges from 60 to 120 m a.s.l. The climate is humid and very humid with cool winter according to Emberger climate classification. Mean annual temperature is 16.33˚C and annual precipitation is 1366.64 mm. Maximum and minimum temperature is 27.8˚C in August and 4.1˚C in February, respectively (data obtained from 1985 to 2005, http://www.weather.ir) (Figure 1). This area is located at about 15 km far away from Rasht, the capital city of Guilan province.

Field sampling Sampling procedure was the systematic random

method. In this method, the sampling network size was 100×200 m. The distances between sampling strips were 200 m and the distances between circular plots on strips were 100 m. Then, start point was randomly selected and the sampling network was systematically located on the map (Poorbabaei et al. 2008; Pourmajidian et al. 2009; Poorbabaei and Poor-rostam 2009; Shafiei et al. 2010). Totally, 89 sampling plots were taken. Data was collected to the class of tree (≥10 cm dbh) and shrub layers (number

of individual) in 1000 m2 circular plots (Zobeiry 2005; Pourmajidian et al. 2009; Shafiei et al. 2010). In the center of these plots, the cover percentage of herbaceous species, including herbs, ferns and mosses, was estimated using Domin criterion by minimal area method with 32 m2 areas. Number of regeneration in two classes include, sapling (≥1.30 m height and ≤10 cm dbh) and seedling (<1.30 m height) were sampled in 100 m2 circular plots. Plant specimens were collected and stored in the Herbarium of Department of Forestry in Faculty of Natural Resources at University of Guilan.

Data analysis Data analysis was carried out using diversity indices of

Shannon-Wiener, Simpson, Mc Arthur’s N1, Hill’s N2, and Smith and Wilson’s evenness (Evar). The diversity indices were calculated separately to different life forms: trees, shrubs, saplings, seedlings and herbs. Indices were used as following (Pitkanen 1998; Krebs 2001; Nagendra 2002; Nangendo et al. 2002; Small and McCarthy 2005; Lamb et al. 2009; Hashemi 2010):

Shannon-Wiener’ H':

Simpson’ 1-D:

Mc Arthur’s N1:

Hill’s N2:

S: the total number of species in the sample. Pi: the proportion of individuals in the ith species (Pi=

ni/N, ni is the number of individuals in the ith species and N is the total number of individuals)

Smith and Wilson’s evenness (Evar) (Krebs 2001;

Gosselin 2006):

Figure 1. Location of the study area: Guilan Rural Heritage Museum, Guilan Province, Islamic Republic of Iran.

Guilan Rural Heritage Museum Islamic Republic of Iran Guilan Province

A AstaraH HashtparBA Bandar AnzaliS SomiehsaraF FoomanR RashtAA Astaneh AshrafiehLh LahijanLr LangeroodRs RoodsarRb RoodbarSh Shaft


184

Arctan: measured as an angle in radians ni: basal area for over-storey species and is coverage for

the under-storey of the ith species in the sampling plot nj: basal area for over-storey species and is coverage for

the under-storey of the jth species in the sampling plot S: total number of species in the entire sample Numbers of species per plot was taken as a measure of

species richness (S) (Timilsina et al. 2007). Data were calculated in Ecological Methodology software (Krebs 2001).

Species importance value (SIV) was calculated for all species by summing relative frequency, relative density and relative dominance values for woody species and summed relative frequency and relative dominance for herbaceous species. SIV was used to identify dominance species in the study area. The following formulas were used for each calculation (Maingi and Marsh 2006; Adam et al. 2007): Relative frequency = Number of plots that contain a species x 100 Number of all plots Relative density = Number of a species in all plots x 100 Total Number of species in all plots Relative dominance = Total basal area of a species in all plots x 100 Total basal area of all species in all plots


Results Totally, 75 plant species including 73 native species

belong to 43 families and 72 genera were recorded throughout the study area (Table 1). Rosaceae and Labiatae families had the highest number of species (Figure 2). Quercus castaneifolia (227.24%) and Ruscus hyrcanus (126.60%) had the highest value of SIV and were the most dominant woody species to tree and shrub layers, respectively. Carex divolsa (76.47%) and Viola odorata (75.80%) were the most dominant herbaceous species. Mean richness of species (S) was higher in herbaceous layer and followed by regeneration, tree and shrub layers (Figure 3). Herbaceous layer had the highest amount of Smith and Wilson’s evenness index (Evar) and followed by shrubs, regeneration and tree layers (Figure 4). Diversity indices of Simpson (1-D), Hill’s N2, Shannon-Wiener (H΄) and Mc Arthur’s N1 in tree, shrub, herbaceous and regeneration layers were showed in Figures 5. Mc Arthur’s N1 was higher diversity index and followed by Hill’s N2, Shannon-Wiener and Simpson in all layers of vegetation cover in the study area.

Table 1. List of plant species in Guilan Rural Heritage Museum.

Family Scientific Name EuphorbiaceaeAcalypha australis L.AceraceaeAcer insigne Boiss.MimosaceaeAlbizia julibrissin Durazz.AlismataceaeAlisma plantago-aquatica L.BetulaceaeAlnus subcordata C. A. Mey.AsteraceaeArtemisia annua L.AspleniaceaeAsplenium adiantum-nigrum L.AthyriaceaeAthyrium fillix-femina (L.) Roth. SalviniaceaeAzola filiculoides Lam.BrachytheciaceaeBrachythecium plumosaCypraceaeCarex divolsa Stokes.BetulaceaeCarpinus betulus L.PapaveraceaeChelidonium majus L.ConvolvulaceaeConvolvulus betoniceafolius Mill. AsteraceaeCorsium arvense (L.) Scop.RosaceaeCrataegus ambigue M. B.PoaceaeCynodon dactylon (L.) Pers. CyperaceaeCyperus rotundus L.LiliaceaeDanae racemosa (L.) Moench.EbenaceaeDiospyros lotus L.OrchidaceaeEpipactis latifolia All.AsteraceaErigeron canadensis L.EuphorbiaceaeEuphorbia amygdaloides L.MoraceaeFicus carica L.RosaceaeFragaria vesca L.RosaceaeGeum heterocarpum Boiss.CaesalpinaceaeGleditschia caspica Dest.AraliaceaeHedera helix L.AraliaceaeHedera pastuchovii Woron. Ex Grossh. HypericaceaeHypericum androsaemum L.HypericaceaeHypericum perforatum L.AquifoliaceaeIlex aquifolium L.JuncaceaeJuncus bufonius L.JuncaceaeJuncus glaucus Ehrh.LabiataeLaminum album L.LabiataeLycopus europaeus L.LabiataeMentha pulegium L.RosaceaeMespilus germanica L.MoraceaeMorus alba L.LabiataeNepeta involucrate (Bunge) Bornm. PoaceaeOplismenus undulatifolius (Ard.) P. OxalidaceaeOxalis corniculata L.BrachytheciaceaePalamocladium sp.HammamelidaceaeParrotia persica C. A. Mey.AsclepiadaceaePeriploca graeca L.VerbenaceaePhyla nodiflora (L.) Greene.AspleniaceaePhylitis scolopendrium (L.) Scop. MniaceaePlagiomnium cuspidatumPolygonaceaePolygonum aviculare L. PolypodiaceaePolypodium vulgare L.SalicaceaePopulus caspica Bornm.RosaceaePotentilla reptans L.PrimulaceaePrimula heterochoroma Starf.LabiataePrunella vulgaris L.RosaceaePrunus domestica L.HypolepidaceaePteridium aquilinum L. Kuhn in Decken. PteridaceaePteris cretica L.JuglandaceaePterocarya fraxinifolia (Lam.) Spach. RosaceaePyrus communis L.FagaceaeQuercus castaneifolia C. A. Mey. RosaceaeRubus persicus Boiss.LiliaceaeRuscus hyrcanus Woron.SalicaceaeSalix alba L.SalicaceaeSalix eagyptiaca L.CaprifoliaceaeSambucus ebulus L.LabiataeScutelaria albida L.PoaceaeSetaria glauca (L.) P. Beauv.LiliaceaeSmilax excelsa L.SolanaceaeSolanum dulcamara L.AsteraceaSolidago virga-aurea L.UlmaceaeUlmus carpinifolia G. Suckow.UrticaceaeUrtica dioica L.CaprifoliaceaeViburnum lantana L.ViolaceaeViola odorata L.UlmaceaeZelkova carpinifolia (Pall.) Dipp.

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Figure 2. Number of species in each family of plants in Guilan Rural Heritage Museum, Iran.

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1.5

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Discussion The assessment of biodiversity in forest has become an

important issue for studying ecosystems and their conservation (Aubert et al. 2003). Biodiversity measurement is recognized as a guidance for conservation plans in local scale. Species biodiversity is used greatly in vegetation studies, and environmental evaluation is one of the main criteria to determine ecosystems condition. So that, many research considered that high species diversity is equal to stability in ecological systems (Mirdavoodi and Zahedi Pour 2005).

The presence of 75 plant species in 260 ha area indicates considerable plant diversity in the study area. Our results showed that herb layer had the highest diversity indices (richness, diversity and evenness). The light penetration was high due to forest disturbance and decreasing canopy coverage, it led to increasing herbaceous species. Also, response of under-storey species to physiographical condition will be used as index of disturbances and changes in environmental and edaphical condition in sites (Mirzaei et al. 2008).

Many studies have emphasized the effects of slopes, aspect and elevation on plant diversity. It seems that high plant diversity in our study area is due to topographic and physiographic condition. This study area is flat in most parts (average of slope in most parts is 0-30 % and in some parts is 30-60%). High plant diversity is also due to fertility and humidity of sites. Steep slopes cause negative effects on site qualities by drainage of available water, soil erosion and decrease of soil nutrients (Sohrabi et al. 2007). In the other hand, low degree of slope and humidity were the most important factors of increasing diversity of herbaceous species (Gholami et al. 2007).

Studies showed that the highest values of richness and evenness occurred in the middle altitudes because of favorable temperature (Mirzaei et al. 2008). Thus, altitude ranging from 60 to 120 m a.s.l in our study area can be an appropriate condition for plant diversity. Northern slopes have more diversity due to must humidity (Kooch et al. 2009). Our study area was flat in many parts but have northern slopes in some parts. This can be evaluated as a reason of acceptable plant diversity.

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Study on the effective environmental condition such as slope, aspects, altitudes and specially edaphic, climatic and anthropogenic factors on plant species diversity should be considered. Mc Arthur's N1 is sensitive to the number of species (Pourbabaei and Ahani 2004). It was the highest value in herbaceous layer due to high number of herbaceous species in the study area. Simpson index is sensitive to the frequency of species (Pourbabaei and Ahani 2004). The highest Simpson index is herb layer, followed by shrub, regeneration and tree layers (shrubs have the lowest number of species but dispersed distributed in the study area). Roberts (2002) showed that fertile sites have the highest value of Hill’s N2 index and this index is significantly higher in natural stands. In our study, value of this index for herb layer was the highest and followed by shrubs, trees and regeneration layers. Comparison of this study area to Gisoom reserved forest in the west of Guilan province (both of them are coastal plain forests in north of Iran) showed that species richness was the same but biodiversity in Gisoom has better condition than in our study area. It seems that conservation strategies are important factor in plant diversity conservation in Gisoom (Ravanbakhsh et al. 2007).

CONCLUSION

Attempts to establish a diverse ecosystem with aesthetic values and help for plant conservation are necessary in Guilan Rural heritage Museum. Diversity is one of the main factors of sustainable forest management. Identifying plants species of a region and their biodiversity is very effective way to identify disturbance factors and develop recovery plans. It is also essential to maintain a high proportion of native woody species, create protection programs and preserve the area against human and livestock disturbances.

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Morphological variation of Hoya multiflora Blume at different habitat type of Bodogol Research Station of Gunung Gede Pangrango National

Park, Indonesia

SRI RAHAYU1,2,♥, MUHAMMAD JUSUF3,4, SUHARSONO3,4, CECEP KUSMANA5, ROCHADI ABDULHADI6 1Department of Biology, School of Graduates, Bogor Agricultural University (IPB). IPB Campus at Darmaga, Bogor 16980, West Java, Indonesia.

2Bogor Botanical Gardens, Indonesian Institute of Sciences. Jl. Ir. H. Juanda 13 Bogor 16911, West Java, Indonesia. Tel. +62-251-8322187 Fax. +62-251-8322187. ♥email: [email protected]

3Department of Biology, Faculty of Mathematics and Natural Sciences, Bogor Agricultural University (IPB), Darmaga, Bogor 16980, West Java, Indonesia

4Research Center for Bioresources and Biotechnology, Bogor Agricultural University (IPB), Darmaga, Bogor 16980, West Java, Indonesia 5Department of Silviculture, Faculty of Forestry, Bogor Agricultural University (IPB), Darmaga, Bogor 16980, West Java, Indonesia.

6Ecological Laboratory, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Cibinong-Bogor 16911, West Java, Indonesia

Manuscript received: 22 June 2010. Revision accepted: 25 October 2010.

ABSTRACT

Rahayu S, Jusuf M, Suharsono, Kusmana C, Abdulhadi R. (2010) Morphological variation of Hoya multiflora Blume at different habitat type of Bodogol Research Station of Gunung Gede Pangrango Natonal Park, Indonesia. Biodiversitas 11: 187-193. Hoya multiflora Blume (Asclepiadaceae) is an Asiatic tropical ephypitic shrub which has been utilized as ornamental plant and reported to possess medicinal properties. The aim of this study was to evaluate the morphological variation of Hoya multiflora populations at the different habitat types of Bodogol Research Station of Gunung Gede Pangrango National Park in Indonesia. We collected 48 samples from three sub populations with six different habitat types. Morphological variation was found in stem, leave, and inflorescence. According to the discriminant and cluster analysis, the 48 samples were separated into three groups at 12 % dissimilarity. The groups were determined by canopy cover degree.

Key words: morphological diversity, Hoya multiflora, Gunung Gede Pangrango National Park.

INTRODUCTION

Hoya multiflora Blume (Asclepiadaceae) is widely distributed throughout India to New Guinea (Hooker 1885; Schlechter 1914; Thaitong 1994), at the elevation of 200-1200 m above sea level (Backer and van der Brink Jr. 1965; Rintz 1980). This species is characterized by its short (non vein) stem, leathery (non succulent) oblong leaves and the flowers have white coronas and yellow/white reflexed corollas (Wanntorp et al 2006). There can be up to 40 of this rocket like flowers in an umbel and they produce lots of nectar, and produces white latex from all of its part.

Hoya multiflora is one of the economically important ornamental plants in the world. In addition, this species has been classified as medicinal plant (Zachos 1998) and its medicinal properties have been used traditionally to treat arthritis-rheumatism (Burkill 2002), and stomach/intestinal ailments (Ambasta 1986) as well. Though the active compound of this plant has not been identified yet, presumably it contains Indomethacin-like compound. It is a common non-steroidal anti-inflammatory drug (NSAID), which has been used for more than 30 years to treat symptomatic pain of arthritis-rheumatism. Recently, this compound has been tested for a new drug as anti HIV

(Bourinbaiar and Lee-Huang 1994), and it seems to be specific since no toxicity has been observed at the IC50 dose.

Despite their high economic importance, little is known about their morphological diversity. The variations of morphological characters provide a range of selection for horticultural purposes, and can also describe the genetic diversity among the populations. Morphological characters are expression of the genetic diversity as interact with their environment. Specific adaptation information will be beneficial for agronomic and horticultural plants which had been and continue to be developed by extensive testing (Vogel et al. 2005). There are some variations on H. multiflora characters according to the geographical range (Goyder 2008). Thus, it is imperative to study the morphological diversity of H. multiflora, especially those which are presence at Gunung Gede Pangrango National Park, Bogor, Indonesia. The H. multiflora populations in this area grow on various habitats and host plants.

The objective of this study is to evaluate the morphological diversity at different habitat types at Bodogol Research Station, Gunung Gede Pangrango National Park, Indonesia.


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Study site There were three subpopulations (Figure 1, red circle)

of H. multiflora at Bodogol Research Station, Gunung Gede Pangrango Natonal Park, West Java, Indonesia used as sample sources. The six different habitat types were identified at the study area. The habitat type was differentiated by its dominant tree, sapling species and canopy cover. The subpopulation-1 has two types of habitat and therefore divided into two sites; the subpopulation-2 has three types of habitat and divided into three sites, and subpopulation-3 only has one habitat type (Figure 1, blue circle). The habitat types of the sampling sites were listed in Table 1.

Plant material Four eight plant samples were collected from the six

different habitat sites at Bodogol Research Station as listed in Table 1. The samples were collected as cuttings for living collection and housed in a shade house at Bogor Agricultural University (IPB), Darmaga, Bogor.

Morphological observation A descriptor list was needed to make a simple

observation. The development of the descriptor was based on the observation of both quantitative and qualitative characters of the vegetative and generative structures. The

describtion of characters terminology are following the “Plant Form” of (Bell and Bryan 2008) and “Botanical Latin” of Stearn (2004). All measurement was in metric and color observation was taken with the Royal Horticulture Society (RHS) color chart (2007).

Data analysis Data analysis consisted of discriminant and cluster analysis

by using SPSS software (Kirkpatrick and Feeney 2005).

RESULT AND DISCUSSION

Morphological variations A descriptor list has been developed as a result of the

preliminary observation as listed in Table 2. Twenty four characters displayed morphological variation among Hoya multiflora populations at Bodogol. Plant growth habit ranged from upright (Figure 2A) and prostrate types (Figure 2B). Node length was ranged from the very short (0.9 cm) to the very long (12.2 cm). These two characters were correlated with the plant performance. The upright plant with short node will give the best performance as pot plant. Leaf blade shape was varied between obovate and oblong, and the intensity of green colour varied from 146 A (yelowish green) to 147 A (green) of RHS color chart standard.

Figure 1. The Hoya multiflora population at Bodogol Research Station, Gunung Gede Pangrango National Park as sample source Table 1. The habitat types of Hoya multiflora populations at Bodogol Research Station, Gunung Gede Pangrango National Park

Sub population Site Habitat type Canopy cover Sample number 1 1 Maesopsis eminii-Cyathea contaminans forest 60.23 % 1,2,3,4,5,6,7,8,9 1 2 Primary mixed forest 61.53 % 10,11,12,13,14,15,16, 17,18,19 2 3 Maesopsis eminii-Calliandra calothyrsus Forest 75.34 % 20,21,22,23,24,25 2 4 Schima wallichii forest 64.15 % 26,27,28,29,30,31,32,33,34 2 5 Ridge open-building mixed 54.62 % 35,36,37,38,39,40,41 3 6 Altingia excelsa Forest 80.23 % 42,43,44,45,46,47,48

6SubPop 3

2

1SubPop 1

SubPop 2

5

43

RAHAYU et al. – Morphological variation of Hoya multiflora Blume

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There were variations on corolla coloration, both on

bud and opened flower stage. Variation between absence and presence on the flower bud anthocyanin coloration was found among the population as presented in Figure 2C and Figure 2D. There were two types of flower coloration among the populations. The pale color (Figure 2E) stated as having two corolla colors and full color (Fig.2F) stated as having one corolla color. Variation was also found at the pedicel length and corolla reflexion (Figure 2G). Pedicel length was varied from 3 cm to 6 cm. Corona type was varied as closed type (Figure 2H) and open type (Figure 2I).

Variation among the observed morpholical characters were performed as expression of the genetic variation among populations in interaction with their environment as adapation process. Genetic change is what occurs in a population when natural selection acts on the genetic variability of the population. By this means, the population adapts genetically to its circumstances (Orr 2005). Populations differ in their phenotypic plasticity, which is the ability of an organism with a given genotype to change its phenotype in response to changes in its habitat, or to its move to a different habitat (Price et al. 2003; Prince 2006). Phenotypic plasticity may occur and first appear at the vegetative characters such as leaf morphology. The morphological variation in leaf shape of Ranunculus repens was concordace by physiological variation in their adaptation to survive at amphibious habitat (Lynn and Waldren 2001; 2003; 2003).

Similarity According to the

discriminant analysis, there were five functions which discriminated the samples (Table 3 and Table 4). The first function with the largest variability explained 45.5% of the among site variation based largerly on six characters namely pedicel anthocyanin, peduncle length, intensity of green color of leaves, corolla colour, leaf blade shape and flower number per umbel. The second function explained 23% of the variation with two main characters namely calyx anthocyanin and pedicel color. The third function explained 14% variation related to six characters i.e. corolla reflextion, corolla number of color, petiole length, corona type, corolla curvature and stem anthocyanin. The first to third functions has cumulatively explained 82.4% of the variation. The fourth function related to four

characters i.e petiole anthocyanin, corolla length, leaves ratio and number of umbel. Then the fifth function related to corolla bud anthocyanin, plant habit, corona length, peduncle anthocyanin, node length and pedicel length. Table 3. Functions at Group Centroids. Function 1 2 3 4 5 Eigenvalue 45.5 23.0 14.0 9.5 8.0 Cumulative % 45.5 68.5 82.4 92.0 100.0 Site 1 -1.075 0.470 0.911 -1.193 -0.469 Site 2 -0.699 0.395 -1.735 -0.136 -0.154 Site 3 1.576 -2.815 0.005 0.007 -0.561 Site 4 -0.194 -0.366 0.262 -0.059 1.444 Site 5 -2.040 0.174 0.675 1.451 -0.402 Site 6 3.319 1.540 0.290 0.347 -0.152 Note: Unstandardized canonical discriminant functions evaluated at group means.

The distribution of samples on a canonical plane was

presented in Figure 3. It was spanned by the first and second canonical axis which in total covered 68.5% of the variation (eigen values). Along the first (horizontal) axis, with eigenvalue equal 45.5%, the samples were separated mostly according to the six characters (pedicel anthocyanin, peduncle length, intensity of leaves green color, corolla color, and leaf shape and flower number per umbel).

Table 2. Characters of descriptor list for Hoya multiflora used in this study

Characters Type of characters

Qualitative character states0 1

1 Plant: habit qualitative upward horizontal 2 Stem: anthocyanin coloration qualitative absent present 3 Node: length quantitative 4 Petiole: length quantitative 5 Petiole: anthocyanin coloration qualitative absent present 6 Leaves: shape qualitative obovate oblong 7 Leaves: ratio width/length quantitative 8 Leaves: intensity of green color of upper part qualitative light * dark * 9 Inflorescence: number of umbel / branch qualitative one more than one10 Inflorescence: number flower / umbel quantitative 11 Peduncle: length quantitative 12 Peduncle: anthocyanin coloration qualitative absent present 13 Pedicel: length at the full opened flower quantitative 14 Pedicel: color at the first open flower qualitative yellow green * green* 15 Pedicel: anthocyanin coloration qualitative absent present 16 Calyx: anthocyanin coloration at the first open flower qualitative absent present 17 Corolla: anthocyanin coloration at the 1st bud qualitative absent present 18 Corolla: number of color qualitative one (flush) two (+white) 19 Corolla: color of lamina tip qualitative yellow * orange* 20 Corolla: length of corolla lobe quantitative 21 Corolla: intensity of reflection qualitative weak medium 22 Corolla: curvature of corolla lobe qualitative weak medium 23 Corona: type qualitative unopened opened 24 Corona: length of corona lobe quantitative Note: * Taken with the Royal Horticulture Society (RHS) Color Chart


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Figure 2. Diversity in inflorescence of Hoya multiflora: a. upright plant b. horizontal plant habit c. absent/very weak in anthocyanin coloration in flower bud d. strong anthocynin in flower bud, e. pale corolla color, f. strong corolla color, g. variation in pedicel length and corolla reflexion. h. closed corona type, i. opened corona type. (Scale: a-b = 5 cm; c-i = 1 cm)

CC=54-65 %CC=80.23 %

SITE

CC=75.34 %

Figure 3. Distribution of samples on canonical plane

The right direction was occupied by site 3 and site 6, which have pedicel anthocyanin coloration, long peduncle, deepest color on leaves and flower, oblong leaves and numerous flowers. The left direction was placed by sites 5, 1 and 2 which possess the opposite characteristic with the sites 3 and 6 i.e. lack of pedicel anthocyanin coloration, short peduncle, lighter color on leaves and flower, ovate leaves and fewer flowers. Sites 3 and 6 were in habitats with dense canopy and site 5 had the most open canopy (Table 1). The canopy density may influence the intensity of green color in leaves. In the condition of dense canopy, the sunlight is weak, which in turn is able to trigger chlorophyl production to catch the more sunlight. Shade plants contain more chlorophyll b or have smaller chlorophyll a:b ratios. At a given nitrogen availability chlorophyll a: b ratios increase with increasing irradiance (Kitajima and Hogan 2003). It is very often observed in the

F

IHG

D E

CBA


191

Table 4. Standardized Canonical Discriminant Function Coefficients and Correlation between Observed Characters and Cannonical Variables of Hoya multiflora

Observed characters

Canonical function 1 2 3 4 5

Canonical discriminant

function coefficients

Corre- lation



Corre- lation



Corre- lation



Corre- lation



Corre- lation

Pedicel anthocyanin 0.980 0.331(*) 0.590 -0.170 -0.718 -0.307 0.168 -0.023 -0.134 -0.045 Peduncle length 10.673 0.250(*) 10.019 -0.067 0.175 -0.063 0.093 0.132 -0.386 -0.244 Leaves green color 0.054 0.150(*) 0.217 0.128 -0.156 0.043 -0.090 0.039 0.304 -0.142 Corolla color 0.560 -0.136(*) -0.319 0.063 0.111 0.106 0.169 0.075 0.751 0.082 Leaves shape -0.173 0.097(*) 10.510 0.040 0.249 0.074 0.013 0.053 -0.296 -0.068 Flower number 10.104 -0.053(*) 0.164 0.002 0.560 0.029 -0.397 0.039 0.014 0.012 Calyx anth ocyanin 0.718 -0.262 10.037 0.299(*) -0.180 0.105 0.712 0.230 0.431 0.020 Pedicel color 0.480 0.089 -0.562 -0.222(*) -0.170 -0.172 0.110 0.050 0.813 -0.002 Corolla reflextion 0.294 -0.035 10.031 0.039 -0.365 -0.282(*) -0.255 -0.032 0.547 -0.043 Corolla number of color 0.296 0.104 0.558 -0.058 0.967 0.275(*) 0.221 -0.170 0.430 0.121 Petiole length -0.621 0.048 10.222 0.063 -0.821 -0.247(*) -0.051 0.083 0.068 0.071 Corona type -0.284 -0.027 0.870 0.181 0.141 -0.223(*) 0.624 0.154 -0.685 -0.076 Corolla curvature -0.927 0.032 -0.307 -0.172 0.058 -0.203(*) 0.139 -0.022 -0.133 -0.146 Stem anthocyanin -0.112 -0.046 -0.949 -0.045 -0.877 -0.154(*) 0.239 -0.049 -0.057 -0.087 Petiole anthocyanin -0.088 -0.236 0.041 -0.054 0.084 0.111 0.635 0.466(*) -0.051 0.101 Corolla length 0.802 0.117 -0.664 -0.060 -0.174 -0.119 0.422 0.210(*) 0.251 0.056 Leaves ratio -0.630 0.078 -0.709 -0.148 0.521 0.015 0.630 0.172(*) 0.071 -0.081 Umbel number -0.127 0.008 -0.191 0.027 -0.385 -0.135 0.437 0.144(*) -0.012 0.104 Corolla bud anthocyanin -0.605 -0.169 0.217 0.069 0.375 0.131 -0.373 -0.057 -0.698 -0.429(*)Plant habit 0.603 0.151 -0.124 -0.048 0.015 0.130 0.484 0.282 -0.071 -0.334(*)Corona length 0.226 -0.053 -0.518 0.059 -0.009 0.008 -0.435 -0.131 0.896 0.251(*) Peduncle antho -0.357 0.042 -0.340 -0.030 0.532 -0.038 -0.370 -0.006 -0.047 -0.193(*)Node length 0.505 0.103 -0.997 0.042 0.650 -0.151 -0.229 0.085 0.620 0.179(*) Pedicel length -0.508 -0.121 -0.301 -0.034 -0.568 -0.095 -0.279 -0.102 -0.437 -0.171(*)Note: * indicate the largest correlation among the five canonical functions for each characters tropics, that individual plants of a given species growing in deep shade inside a forest and exposed to full sun-light in an open habitat respectively, form morphologically very different phenotypes, which are also strongly distinguished by pigmentation especially as a respon to photosynthetic apparatus (Lutge 2008).

The plants living in a shade and humid area have been predicted to have more nutrients to be absorbs so will affect on the growth (peduncle length, leaves size and number of flower). This condition is identical with the experiment result of Issarakraisila and Settapakdee (2008) on the seedling of Garcinia mangostana as a shade tolerant plant. An increase of light intensity increased the thickness of lamina resulting in an increase of palisade and spongy tissues and the stomata frequency also increased. Both chlorophyll a and b declined gradually as the light intensity increased and the average ratio was 0.808. The growth of seedlings described as leaf size, leaf number per plant, total leaf area, height, fresh weight and dry weight were dramatically reduced when exposed to 100% light intensity condition. Maximum growth was found when exposed to 40% light intensity condition. Clones of population native to shade and to exposed environments show differences in the photosynthetic response to light intensity during growth (Björkman and Holmgren 2006).

So far, the samples were grouped based on their morphological similarities. As shown in Figure 3, there were three clusters of 48 samples from the six sites. The first cluster was consist of all samples from site 6 at the

above right of the plane, the second was consist of samples of site 3 at the below of the plane, and the third was consist of samples from sites 5, 2, 1 and 4 at the above left of the plane. This result was identical to the result of a cluster analysis by using mean coordinates on the five canonical axis (Table 3). A dendogram displayed on Figure 4 showed the separation of six sites into three groups at 12% dissimilarity level. The first group was site 6, the second was site 3 and the third was consisting of sites 5, 2, 4 and 1. Sites 5, 2, 4, and 1 possess dissimilarity at below 5%.

C A S E 0 5 10 15 20 25

Label Num +---------+---------+---------+---------+---------+

1,00 1

5,00 5

2,00 2

4,00 4

3,00 3

6,00 6

Figure 4. Dendogram of 6 groups of Hoya multiflora population, generated from canonical coordinate of means.


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The similarity between six sites was performed by morphological characters, which were discriminated by its different habitat. According to the analysis the sites 5, 2, 4, and 1 were similar at 95%, while sites 6 and 3 were separated at 12% dissimilarity level. Their similarity degree was match with the canopy cover (Table 1). Sites 6 and 3 occupied dense canopy cover (80.23% and 75.34%), while the other sites at medium canopy cover (from 54-64%). These six sites were different in dominant tree species, however the four sites (5, 2, 1, and 4) have relatively similar habitat, particularly on the degree of canopy cover (from 54.62% to 64.51%). It was means that morphological variations among the samples were influenced by the environment, especially the degree of canopy cover. Light intensity is the most factors related to the canopy cover. According to Luttge (2008), light is one of the environmental important factors in the tropical forest that become a stress factor which support such phenotypic variability in relation to plasticity. Phenotypes are the receivers and modulators of environmental input and producers of output performance at the community level.

Plants may be genetically determined for growth at low or high light intensity. However, there are also ontogenetic and developmental modifications, where light exerts a signalling function rather than being only the energy source of photosynthesis, and plants may acclimate or adapt ecophysiologically to low and high irradiance, respectively (Lutge 2008). The potential for light acclimation is species specific and may involve major structural and functional changes in the photosynthetic apparatus (Bailey et al. 2001). In sun plants increased chlorophyll a/b ratios and a comparatively small size of chlorophyll a and b binding antennae contribute to protection from too high irradiance (Krause et al. 2001). Plants permanently exposed to full sunlight have effective protectivemechanisms (Krause et al. 2006). The understory shrub C. glabellus shows the distinct differences between sun and shade plants. Shade plants have lower leaf conductance to water vapour, gH2O, than sun plants which leads to lower gas exchange and growth (Bonal et al. 2000; Sack et al. 2005).

Phenotypic plasticity must be considered in relation to co-occurrence of different genotypes within a population which are each adapted to a slightly different environment. Genetic variation is reflected in phenotypic plasticity (Booy et al. 2000). Plasticity itself can be considered as a trait, which is subject to selection (West-Eberhard 1989). However, plasticity per se is not adaptive. Adaptive plasticity in plants is commonly interpreted for fitness estimates like size and fecundity. The specialization hypothesis, however, predicts that plasticity in such characters is not a product of selection but, rather, a product of specialized (i.e., ecotypic) adaptation to particular environmental condition (Lortie and Aarssen 1996). This much depends on the physiological costs of plasticity (van Kleunen and Fischer 2005). In any case, phenotypic plasticity offers material for selection, since selection is acting on the phenotypes. Thus, the promotion of phenotypic plasticity by variable and medium stress may be one of the reasons for the extraordinarily high biodiversity of tropical forests (Lüttge 2008).

CONCLUSION

Variation on morphological characters was found in Hoya multiflora populations at Bodogol Research Station of Gunung Gede Pangrango National Park, Indonesia. The variation was found in stem, leaves, and inflorescence of the samples among six different habitat types. According to the discriminant and cluster analysis, the six sites were separated into three groups at 15 % dissimilarity. The similarity of habitat was performed by its canopy cover degree rather than dominant tree species. The first group had the highest canopy cover (80.23%) having dominant characters i.e. pedicel anthocyanin coloration, long peduncle, deepest color on leaves and flower, oblong leaves and numerous flowers. The second group with the canopy cover of 75.34% was characterized by intermediate morphological characters, and the third group, which included four sites (sites 5, 2, 1 and 4) with low canopy cover (54.62%-64.15%) had intermediate and lowest morphological characters.

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The effects of forest burning and logging toward regeneration ability of Sowang (Xanthostemon novaguineense Valet.) in Cycloop Mountain,

Jayapura, Papua

SRI WILUJENG♥

Biology Program, Department of Mathematics and Natural Sciences Education, Faculty of Teacher Training and Education Science, Cendrawasih University. Jl. Raya Sentani-Abepura, Jayapura 99351, Papua, Indonesia. Tel./Fax. +62-0967- 582806, +62-0967-587713. ♥email:

[email protected]

Manuscript received: 17 June 2010. Revision accepted: 4 August 2010.

ABSTRACT

Wilujeng S (2010) The effects of forest burning and logging toward regeneration ability of Sowang (Xanthostemon novaguineense Valet.) in Cycloop Mountain, Jayapura, Papua. Biodiversitas 11: 194-199. Sowang (Xanthostemon novaguineense Valet.) is an endemic plant of New Guinea Island, which is threatened by human activities through land conversion, forest burning and logging. This research aims to know the Sowang developmental phase and stem branching, seedling dominance level, and effect of environmental factor alteration towards the amount of Sowang seedlings at burning and logging areas, and natural forest as control parameters. Sowang stem, derived from shoot of burning area, grows branchy from the lower part of stem. Sowang stem derived from seed grows monopodially. Sowang seedling, derived from stem shoot of burning area, have already started flowering phase that occurs all seasons. Individual of Sowang, derived from seed of logging area and natural forest,flowers on the tree level once a year. Sowang seedling became dominant species at burning area. Environmental factors affect Sowang seedling population density were crown covering and light intensity.

Key words: population, Sowang, Xanthostemon novaguineense, branching, flowering, domination.

INTRODUCTION

Papua is one of Indonesia’s islands that have a high biological diversity and endemic level. Papua is estimated contains almost half of the Indonesia’s biological diversity assets. Papua’s endemic species, which is mostly used by the local people, is vascular plant species, e.g. Sowang (Xanthostemon novaguineense Valet.) (Figure 1). Sowang is a fire-resistant plant, and its wood quality belongs to the category of sea wooden gimlet resistant. Until now, scientific information about Sowang is still rare. This is supported by statement of Wilson and Pitisopa (2007) that X. novaguineense is an endemic plant of western Papua New Guinea Island with limited available site data.

Sowang’s habitat area in Jayapura exists at Cycloop Mountain. Sowang grows at the west, south, east, and is an endemic plant of New Guinea Island. Cycloop Mountain lies alongside at the north of Jayapura. Sowang’s habitat is a lowland at 15-450 meters above sea level. That is why Sowang are found abundant at the foothill of Cycloop Mountain or at another area except natural preserve area. The wide of those Sowang’s habitats then decrease because of land conversion and forest yield exploitation, and the rest of it are still being a traditional forest that is authorized by traditional citizens.

Traditional people lives at the west of Cycloop

Mountain. Their activities in the forest include repeatedly burn and log trees. Meanwhile, south to east area of Cycloop Mountain is a forest product exploitation and land conversion area. It is causing the south to east side of Cycloop Mountain undergoes land damage and conversion that make it become no longer conducive for Sowang population. Yepasedanya (2004) wrote that traditional citizens and society has divided Cycloop area become the zones of residential, farming, forest yield collecting area, and traditional restriction (natural forest).

Sowang’s resistant toward fire is a form of self-defense to survive in ecosystem. This self-defense effort affects Sowang branching and developmental phase. In this case, Sowang branching and developmental phase is tightly related with the regeneration ability. Besides qualitative methods above, there is a need of quantitative indicator to show Sowang population ability of self-defense to survive from extinction. The threat to extinction particularly comes from the disruption activities by local people through forest burning and logging. The indicator explained above was a dominance level, which was analyzed using Importance Value Index (IVI) of seedling and an affect of environmental factor toward individual amount of Sowang seedling. Environmental factor, which were observed, are crown covering, light intensity, air temperature, soil temperature, humidity, soil moisture, and soil pH.

WILUJENG – Regeneration ability of Xanthostemon novaguineense

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A

B C D

Figure 1. Xanthostemon novaguineense Valet. A. Regenerant in the burning area (three years old), B. Flower, C. Fruits, D. Leaf. Bar = 5 cm.


Time and area study This research was performed in Doyo Baru, Sub

District of Waibu and Maribu, and Sub District of Sentani Barat, District of Jayapura, Papua. The research location is kind of unfolded area of tropical forest ecosystem. The forest in Doyo Baru is a secondary forest that is deliberately burned repeatedly. The last burning was performed ± 3 years before this research. After the last burning, BKSDA (Nature Conservation Agency) of Papua planted Podocarpus neriifolia and Anacardium occidentale species as reforestation plants.

Because of its same unfolded area, species existed before the burning and logging were assumed alike with species at the natural forest. By the traditional society,

forest at Maribu is divided into forest for logging activity and natural forest. Logging area is a natural forest which the pillars and the trees are cut selectively, so the crown covering still dense. Tree species that are cut are X. novaguineense, Calophyllum sp., Pometia sp., Homalium foetidum dan Intsia bijuga. If the pillar and tree level of those species are totally cut in one area, logging activity will be moved to another area at the same forest. At the sampling location, the last logging was done ± 3 years ago.

Study design The research was designed with quasi-experiment.

Natural forest was assumed as control. Sample acquisition was performed in Kampung Doyo Baru to represent burning area, and at Kampung Maribu to represent logging area and natural forest. The sampling area has an 85-142


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meters above sea level, the height level was measured with altimeter while clinometer was used to measure the slope. The last time of burning and logging activities is ± 3 years.

Procedures The methods of data collection for testing are

categorized into three steps, (i) branching and development phase of Sowang, (ii) Importance Value Index (IVI), (iii) the effect of environmental factor towards Sowang seedling. In first step, branching and developmental phase of Sowang, observations branching and flowering period of Sowang were done. The observations that performed comprised were: (i) sowang branching from seed and stem shoot in the burning area, logging area, and natural forest; (ii) flowering phase and flowering frequency of Sowang individual from seed and stem shoot in the burning area, logging area, and natural forest.

The second step was to find the Importance Value Index (IVI). Sampling unit was a transect line with sampling plot sited crossly at the left and right parts of line, with 10 meters length between plot. Transect placing was done systematically with regarded of the border affect. Plot placing in the burning and logging areas were determined by the estimate of same land height and last time in logging and burning activity. Meanwhile, plot determination in natural forest was conducted based on the height level approximation of the same places.

Each sampling area was assumed homogeneous because there are a limitation in the last time of burning, logging, and the limitation of land height. Sampling size for each sampling area proportionally appropriated with the wide of each sampling area. It is estimated that the wide of burning area is 20 ha, logging area is 30 ha, and natural forest is 50 ha. There were two tracks of transect at the burning area, which each had a 110 meters and 100 meters length between tracks, 20 sample plots are obtained. Transect direction was upright of contour. At the logging area, there were three tracks of transect, which had a 110 meters length for each and entirely 30 sample plots. At the natural forest, there were five tracks with the length was 110 meters for each, 50 sample plots are obtained entirely. In the logging area and natural forest, transect direction was upright towards river stream direction. Tree community analysis of vegetation was done to gain the importance value for Sowang seedling population. Sampling technique was set by determine 2 meters x 2 meters, and bordered using measure tape. Data collection technique included individual and type census for every plot. Vegetations that been found were collected as herbarium, for identification requirement. Stand criteria for tree plants, which were, belong to the seedling class was ≤ 1.5 meter height.

The last step was collecting data to determine the effect of environmental factor towards Sowang seedling. Data collecting was done in the sampling plots sized 10 meters x 10 meters at transect with no regarded to the border affect. Transect was placed at the burning area, logging area, and natural forest systematically in two tracks. The data, which were taken, were: (i) crown covering (%), which was measured by comparing the wide of crown opening area

with the plot area. The crown covering percentage per plot is a unit data of experiment; (ii) light intensity (Wm-2), the measurements were performed on land surface at 12.00-13.00 o’clock. The measurements used lux-meter in every corner and center of plots. The average of light intensity that was obtained per plot is a unit data of experiment; (iii) air temperature (ºC), with determinations of daily temperatures were done 2 times a day, 08.00 and 16.00 o’clock in every plot. The air temperature measurements were performed with thermometer placed under the crown (± 0.5 above land surface) in every corner and center of plots. The average of air temperatures per plot is a unit data of experiment; (iv) soil temperature (ºC), the measurements of soil temperature were performed in ± 30 cm depth with 3 times repetition in every plot. The average of soil temperatures per plot is a unit data of experiment; (v) humidity (%), the humidity measurements were performed 2 times a day, which were 08.00 and 16.00 o’clock in every plot. The measurements were done using hygrometer placed under the crown (± 0.5 m above land surface) in every corner and center of plots. The average of humidity per plot is a unit data of experiment; (vi) soil moisture (%), the measurements were performed by soil sampling in ± 30 cm depth compositely with 3 times repetition in every plot. The water content calculation was performed by gravimetric, using oven and weights. The percentage of soil moisture per plot is a unit data of experiment; (vii) soil pH, the measurements were performed directly by soil pH meter in ± 30 cm depth. Repetitions were done 3 times in every plot. The average of soil pH per plot is a unit data of experiment; (viii) population density (individual amount) of breeds, the calculations of individual amount of Sowang breed were performed in every plot. The amount of breed individual in every plot is a unit data of experiment.

Data analysis To interpret the obtained data, the following tests were

done: (i) branching and developmental phase of Sowang,. qualitative data of branching and developmental phase of Sowang from seed and stem shoot at the burning area, logging area, and natural forest was tested by descriptive analysis; (ii) Importance Value Index (IVI), IVI are counted with the formula IVI = Rd + Rf, with the components are Relative density (Rd) and Relative frequency (Rf). Rd is a proportion between the individual total of certain species with individual total of all species in sampling units. Rf is a proportion between certain species frequency with total frequency of all species in sampling units. The calculation of Rd and Rf values was performed toward each of tree plant species in sampling units. IVI values of all species were calculated in every burning area, logging area, and natural forest; (iii) the effect of environmental factor towards seedling population density, the difference of environmental factor in the burning area, logging area, and natural forest were showed by Analysis of Variance (ANOVA) and LSD α 0.05 through the model:

Yij = µ + ρi + Єij; and LSD α .,05 = t α 0.05 (2 s²/r)1/2


197

Multiple regression analysis was used to show the effect of environmental factor towards seedling population density. The equation model of doubled regression analysis is formulated as: Yi = b0 + b1xi1+ b2x i2+ b3x i3 + b4x i4 + b5x i5 + b6x i6 + b7x i7

Multicollinearity test was used by correlation analysis

of inter free variable. If multicollinearity occurred, one of the variables will be rejected.


Branching and developmental phase of Sowang Sowang includes in Myrtacea family. Sowang is a type

of plant, which shoot will be able to grow after its above-ground-stem is cut or burned. More than one shoots or branches will be growth from the trunk. This branching is not a monopodial type as the Sowang individual growth from seed because the primary stem stops the growth. According to research result of Wilson (2000), lateral bud or branch growth on the direct sun lighted plant are stimulated by activity of cytokinin hormone concurrently with sunlight stressing on the activity of auxin hormone to trigger the development of primary stem.

Myrtaceae has an amount of fire-resistant plant genus. Study results by Burrows (2002) show that genus of Angophora, Eucalyptus, and Lophostemon has an epicormic bud which able to produce stem and branch after burned. An epicormic shoot is a bud under the bark of a stem or branch of a plant, or a shoot (water sprout) growing from such a bud. Epicormic buds lie dormant beneath the bark, their growth suppressed by hormones from active shoots higher up the plant. Under certain conditions, they develop into active shoots such conditions may include damage to higher parts of the plant, or increased light levels following removal of nearby plants.

Dormant axillary buds allow plants to repair minor damage to their canopies. In woody plants, these buds subsequently develop into epicormic structures that may allow vegetative recovery after major disturbances. All investigated Myrtaceae species had an excellent meristem reserve for recovery of photosynthetic capacity after minor canopy damage and for developing epicormic structures for sprouting after more severe damage (Burrows, et al. 2008).

In this territory, all burning residual stem able to grow shoot. Sowang derived from this stem shoot are able to flowering despite still on the seedling size. Resultant flower can produce fertile seed. Flowering phase is occurred all seasons. Small and light seed ejected from fruit split on the tree reinforces the assumption that seeds are spread by wind. Due to the statement of Sera and Sery (2004) that the plants that produce much seeds with relatively small size generally spread the seeds by wind.

Sowang is much more found in gardening zone. Gardening zone is an area which undergo repeated burning. It cause Sowang never grow to be adult phase in gardening zone. This is congruent with result of the research of Hoffmann et al. (2003) which shows that individual

productivity of tropical forest is about 2 times compared with savanna individual, but need longer time to reach production maturity in successive forest burning if the interval of burning time is short.

Maribu is a sampling area for logging area and natural forest. Here, logging activity is selectively performed to take woods based on needs. Sowang wood is taken only for special concern such as for house pillars of tribal chief. Logging activity is impossible to be performed if the wood wants to be taken in the tree dimension, so the tree should first be downed by burning its root. Therefore, there is no trunk remained from Sowang tree for shoot to grow. In the natural forest, none of the individual of Sowang is found derive from shoot, all of them are derived from seed.

In the logging area and natural forest, pillar sized Sowang and Sowang tree derived from seed are not in flowering. Flowering frequency is occurred once a year. This is due to the observation of Australian National Botanic Gardens (2003) that X. verticillatus natural flowering time is spring, but in the glasshouses at the Australian National Botanic Gardens it flowers all year round with masses of flowers all summer. Flowering is enhanced with warmth and high light intensity.

Branching of Sowang, which is derived from side-widen stem shoot at low-level land, is placing Sowang seeds on growth media (soil) which appropriate with germination requisite of Sowang seed. At that condition, plus with the frequency different of flowering, Sowang from stem shoot produces more seedlings than Sowang from seed. Seed from Sowang derived from seed has low probability to stick on appropriate and ‘desired’ growth media in the case of its mild weight and dependence on wind direction.

Importance Value Index (IVI) Analysis resulted eight tree species, which had highest

seedling IVI at each sampling area. Analysis results then compared by tabulation with dominance level of Sowang seedling in Table 1. Table 1 indicates that Sowang seedling population at burning area was dominance population in its community. In the burning area and natural forest, Sowang seedling was not included into dominance population, moreover, not found in the logging area.

Ex-burning area is a suitable environment for Sowang germination and seedling live, proved by Sowang seedling’s high IVI. Only certain plant can live after burning event. This phenomenon shows that environmental factors in this area fulfill the needs for Sowang germination, also for its seedling growth and branch out. A certain species can be dominant if it able to use the environmental factor so that affect community. According to Richards et al. (2003), Xanthostemon belongs the genus that has the low photosynthesis activity, high transpiration rate, and needs high concentrate Mn. X. formosus species needs water in great amount, for that reason this species easily found in the riverside. Meanwhile, X. chrysanthus ables to grow under various environments, although it is naturally found in riparian rain forest. On the other hand, Woinarski et al. (2000) report X. paradoxus in Australia has its best habitat in open forest.


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Table 1. Highest seedling IVI of tree species and Sowang seedling IVI in the burning area, logging area, and natural forest.

Sampling area Species Rd (%)

Rf (%)

IVI(%)

Burning area Podocarpus neriifolia Xanthostemon novaguineense Stenocarpus leccari Decaspermum fruticosum Gordonia papuana Anacardium occidentale Rhodomyrtus sp. Casuarina rumphiana

33302741111

3737733333

70673474444

Logging area Pometia pinnata Mallotus sp. Calophyllum sp. Intsia bijuga Rhodomyrtus sp. Alstonia scholaris Eugenia sp. Syzygium sp.

67566546

65655554

1212111111109

10Xanthostemon novaguineense 0 0 0

Natural forest Calophyllum sp. Litsea sp. Rhodomyrtus sp. Xanthostemon novaguineense Canarium sp. Diospyros sp. Pometia pinnata Elaeocarpus sp.

1523444322

151533444

3024977766

Although Sowang breed is able to compete with

introduced Anacardium occidentale, it is not yet able to equal the domination. Podocarpus neriifolia is also introduced as a greening plant. The worry that Podocarpus neriifolia become the threat for Sowang domination can be occurred, as it is happened in X. verdigonianum and X. philippinensis in Philippines. Baguinon et al. (2003) explained that X. verdigonianum and X. philippinensis are endemic species in Philippines. These species grow unhealthy on ultrabasic land. Ultrabasic land is not optimum environment for those species. It is worried that those endemic species cannot compete with an introduced exotic species. The introduced species is a reforestation plant that has a wide tolerant interval toward environmental factor.

In addition, there was a different of seedling species, which dominated burning area, logging area, and natural forest. If assumed that natural forest is a control area, environmental change resulted of human behavior and activity was occurred in the burning and logging area. This is congruent with the research by Bischoff et al. (2005) concerning secondary succession caused by forest logging in Dipterocarpaceae Kalimantan forest. The research results show that logging can cause the secondary succession. Secondary succession in the lowland of Dipterocarpaceae Kalimantan rainforest is affected by conversion sequence of primary forest after reforestation. The succession process that is happened depends on the composition of remain plant species and the invasion of plant species from outside. These situations show the uncertainty of which type of forest will be growth.

Table 1 also shows that difference of dominant breed species is much more found in burning area if it is compared with control area, which was natural forest. This phenomena is supported by the statement of Stolle and Lambin (2003) that the influence of flamed forest is greater than logging activity, which fire negatively affects species diversity. However, in long-term condition, the remain of unfired forest can be used as one of the source for tree species spreading which locally extinct by burning event. This is supported by statement of Platt and Connel (2003), that the consequences of fire disruption has a similar effect to natural disturbances. This disruption will cause significant changes that will form the natural variability in species composition.

The effect of environmental factor towards the amount of Sowang seedling

ANOVA and LSD α 0.05 results for the effect of environmental factor towards the amount of Sowang seedling are showed in Table 2.

Percentage decreasing of crown covering in the burning area is followed by increasing of light intensity, air temperature, and soil temperature, and decreasing of humidity. Soil moisture in these three sampling area are not show significant different, environmental factor of underground plant generally has changed with relative slow fluctuation. The change of soil pH which burning and logging area’s pH is lower than at natural forest was caused by decreasing of humus partly washed by burning event, included alkali cations. An observation by Handayani and Prawito (2002) on post deforestation land in Bengkulu, Sumatra, showed there are significant differences between the post combustion logging soil and the forest soil pH. Post combustion logging soil pH is 5.48, lower than forest soil pH, 6.4. This is appropriately fit to the research result of Markewitz et al. (2004) which said need a long time to increase soil pH to the initial state in Amazonia secondary forest after burning.

In multicollinearity analysis between freedom variables, there are correlation coefficient score 0.923, 0.590, and 0.501 between crown covering with light intensity, air temperature with humidity, and air temperature with soil temperature. In the case of its effect is assumed equal, further analysis will use light intensity and air temperature variables. Analysis results are showed in Table 3.

Table 3. Multiple regression coefficient of the effect of environmental factor towards the individual amount of Sowang seedling.

Variables B Sig.

Constant value Light intensity Air temperature Soil pH

17.683 0.015 −1.394 3.342

0.610 0.000 0.244 0.283

Regression equation obtained is: Y = 17.683 + 0.015x2

- 1.394x3 + 3.342x7, R² = 0.404. In the degree of confident 99%, light intensity and crown covering affect the


199

individual amount of Sowang seedling. The individual amount of Sowang seedling will rise if an escalation of light intensity is occurred. On the other hand, the increase of crown covering causes the decrease of Sowang seedling amount. Franklin et al. (2005) noted that light intensity is amongst the most important environmental cues regulating plant development. In addition to light quantity, plants measure the quality, direction and periodicity of incident light and use the information to optimise growth and development to the prevailing environmental conditions. The research results of Pearson, et al. (2002) also showed that the percent germination of seeds of pioneer plants in Panama is influenced by light intensity and seed's mass but not influenced by fluctuations in the surrounding temperature.

Environmental and genetic factors give a large influence in population growth of certain species. The principle of Berryman (2003) said that every population grows with the constant rate logarithmically, except if it is influenced by other power or energy in its environment. Dynamic prediction of population is defined as a deviation of function value from biotic factor, abiotic factor, and genetic trait. This fact is occurred in Acacia rigens, A. wilhelmiana, Triodia scariosa, and Eucalyptus sp., mainly by the environmental influence. The research results by Cohn and Bradstock (2000) show that the frequency increase of low precipitation with weeds consumption interaction by herbivore decreases the germination ability of species seeds. This event causes rareness of the former species in latest 8 years. In the remain of burning area at the foothill of Cycloop Mountain, that event is not occurred in Sowang species. It shows that the environment with the post-burning environmental factor is an optimum environment for the germination of Sowang seeds.

CONCLUSIONS

Sowang branching derived from shoot in the burning area shows halted growth of primary stem. Sowang stem derived from seed grows monopodially. Sowang seedling and stake derived from stem shoot in the burning area has entered the flowering phase, which are occurred all seasons. Sowang derived from seed in the logging area and natural forest is flowering in the tree level for once a year.

Sowang seedling’s IVI in the burning area is higher than in logging area and natural forest. Environmental factors, which affect the amount of Sowang seedling were light intensity and crown covering. The amount of Sowang seedling will rise if the increase of light intensity is occurred. On the other hand, the increase of crown covering causes the decrease of Sowang seedling amount.

REFERENCES

Australian National Botanic Gardens (2003) Xanthostemon verticillatus. www.anbg.gov.au Baguinon NT, Quimado MO, Fracisco GJ (2003)

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Berryman, AA (2003) On principles, laws and theory in population ecology. Oikos 103: 695-701

Bischoff W, Newbery DM, Lingenfelder M, Schnaeckel R, Petol GH, Madani L, Ridsdale CE (2005) Secondary succession and dipterocarp recruitment in bornean rain forest after logging. Forest Ecol Manag 218: 174-192

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Burrows GE, Hornby SK, Waters DA, Bellairs SM, Prior LD, Bowman DMJS (2008) Leaf axil anatomy and bud reserves in 21 Myrtaceae species from Northerm Australia. Int J Plant Sci 169 (9): 1174-1186

Cohn JS, Bradstock RA (2000) Factors affecting post-fire seedling establisment of selected mallee understorey species. Aust J Bot 48 (1): 59-70.

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Handayani IP, Prawito P (2002) Post deforestation land in Bengkulu, Sumatera. Jurnal ilmu-ilmu Pertanian Indonesia 4 (1): 1-9.

Hoffmann WA, Orthen B, Nascimento PKVd (2003) Comparative fire ecology of tropical savanna and forest trees. Funct Ecol 17 (6): 720-726

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Table 2. Crown covering average, light intensity, air temperature, soil temperature, humidity, soil moisture, and soil pH in the burning area, logging area, and natural forest. Environmental factor Burning area Logging area Natural forest

Crown covering (%) 20.526±6.06 b 72.143±12.48a 68.000±20.46a Light intensity (Wm-2) 1542.105±208.44a 357.143±175.04b 555.556±399.62bAir temperature (ºC) 31.737±0.85a 28.571±0.73b 29.333±0.86b Soil temperature (ºC) 29.105±1.06a 26.143±0.35b 26.000±0.38b Humidity (%) 53.368±2.92b 68.000±6.90a 65.444±4.31a Soil moisture (%) 35.084±2.46a 35.447±9.99a 33.292±9.44a Soil pH 6.000±0.36b 5.786±0.50b 6.678±0.32a Note: that average values followed by same letter at the same row is not significant at LSD α 0.05


Recognition of seasonal effect on captive Sumatran Sambar deer reproductive cyclicity and sexual behaviors

HERI DWI PUTRANTO1,2,♥, EDI SOETRISNO1, NURMEILIASARI1, AHMAD ZUENI2, BERRY GIBSON2 1 Department of Animal Science, Faculty of Agriculture, University of Bengkulu, Jl. W. R. Supratman, Kandang Limun, Bengkulu 38371A, Indonesia,

Tel. +62-736-21170 ext. 219, Fax. +62-736-21290, ♥email: [email protected] 2 Graduate School of Natural Resources and Environmental Management (PPs-PSL), Faculty of Agriculture, University of Bengkulu, Jl. W. R.

Supratman, Kandang Limun, Bengkulu 38371A, Indonesia

Manuscript received: 2 August 2010. Revision accepted: 6 September 2010.

ABSTRACT

Putranto HD, Soetrisno E, Nurmeiliasari, Zueni A, Gibson B (2010) Recognition of seasonal effect on captive Sumatran Sambar deer reproductive cyclicity and sexual behaviors. Biodiversitas 11: 200-203. The objective of this study was to identify seasonal effect on reproductive cyclicity of a captive female Sumatran sambar deer by monitoring its visual estrus manifestations and visual sexual behaviors in buck during female natural estrus in ex situ habitat. A pair of six years of age Sumatran sambar deer was used in this study. Daily observation of visual estrus manifestations of doe and visual sexual behaviors of buck was conducted using focal-animal sampling by two animal keepers during 0800 to 1700 h from June-July 2009 (dry season) to August-September 2009 (rainy season). Doe visual estrus manifestations include apparent reddening and swelling of the external genitalia, loss of appetite and a natural tendency of the doe to approach the buck. There was no significant effect of season on doe visual estrus manifestations and buck sexual behaviors (p > 0.05), except for loss of appetite and fighting behavior, respectively. Estrus was observed monthly and result of the cycle was 25.00 ± 5.22 days. It is possible to assess non-invasively estrous cycle of Sumatran sambar deer by the observation of visual estrus manifestations and there was less of seasonal effect on doe-buck sexual behaviors during female natural estrus in ex situ habitat. Key words: estrous cycle, sambar deer, seasonal effect, sexual behavior.

INTRODUCTION

Indonesia is a habitat for eight sub-species of Cervus timorensis, two sub-species of Cervus unicolor, and Axis-axis (Semiadi and Nugraha 2004; Garsetiasih and Takandjandji 2006). C. unicolor which is known as sambar deer, inhabits some areas in Asia and Australia. Moreover, a sub-species of sambar deer (Cervus unicolor Equinus) is an endemic deer populated in Bengkulu province, particularly in Kerinci Seblat National Park (TNKS), Sumatra island of Indonesia. Sumatran sambar deer inhabit TNKS, that a total of 22.73 % of TNKS territorial area are located in Bengkulu province (Putranto et al. 2008, 2010; Soetrisno et al. 2009).

In Oceania, Asia and Europe Union countries, deer has been domesticated (Gordon 2004), and venison becomes an alternative of natural protein resources for the society. Unfortunately, the demand of venison in Indonesia nowadays is fully supplied by poacher hunt, even though deer is classified into Lower Risk/Least Concern by 2007 IUCN The Red List of Threatened Species (IUCN 2007), then Vulnerable by 2010 (IUCN 2010). As a result, deer in situ population in Indonesia decreased gradually due to poaching and over hunting (Takandjandji and Garsetiasih 2002; Garsetiasih and Takandjandji 2006; Soetrisno et al. 2009; Putranto et al. 2010).

Recently, the population of sambar deer in their habitat is not recorded. Furthermore, captivity program or intensive domestication of sambar deer in Indonesia is not as popular as in other countries such as Australia, Malaysia and Thailand (Semiadi et al. 2005), while the venison consumption among native Indonesian society is common (Mukhtar and Suita 2002; Semiadi 2002). In fact, there is only one captive sambar deer preservation recorded, that is located in East Kalimantan province (Muchsinin et al. 2002).

In order to improve the Sumatran sambar deer population in situ and ex situ, it requires the breeding performance and reproductive physiology information of sambar deers. There are limited scientific references on the reproductive physiology and endocrinology of sambar deer (Soetrisno et al. 2009; Putranto et al. 2010). In the last five decades, there have been seven reports on general management and biology of sambar deer (Van Mourik and Schurig 1985; Semiadi et al. 1993; Semiadi et al. 1994; Ahmed and Sarker 2002; Muchsinin et al. 2002; Semiadi et al. 2005; Putranto et al. 2010). However, there is only a report on its breeding record (Awal et al. 1992).

Sambar deers reach sexual maturity at 8 months of age and its life span which is up to 11 years in the wild (Jacoeb and Wiryosuhanto 1994). In general, deer breeding occurs from October to January with peak activity in November. Does are in heat for 24 hours every 28 days for 2 to 3 consecutive cycles. Single fawn is born every 2 to 3 years

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after a gestation of 7 months, and the peak of fawn drop in May or June (Craven and Hygnstrom 1994).

Characteristically, Sumatran sambar deer (C. unicolor) is categorized as a ruminant species with specific behavior and different to other ruminants. Sambar deer has a very sensitive hearing capability as well as a sensitive sense of smelling and high speed movement (running and jumping) (Putranto et al. 2010). However, does an intensive management system at ex-situ habitat can diminish sambar deer natural behavior especially their breeding behaviors? It would be a chance for scientist and conservationist for a further exploration.

Season has a great impact on animal reproduction. In a temperate zone, white-tailed deer (Odocoileus virginianus) is a breeding season deer (Li et al. 2001). However, in a tropical zone breeding may take place any time of the year. Indonesia which is dry and rainy season periods in tropical zone it may affect the endemic mammals production performances and reproduction status such as Sumatran sambar deer. Therefore, there is an urgent need to discover the Indonesian tropic seasonal effect on sambar deer reproduction status and sexual behavior to support the conservation program.

The purpose of the present study was to identify the seasonal effect (dry and rainy season) on reproductive cyclicity of individual female Sumatran sambar deer by monitoring the visual estrus manifestations and visual sexual behaviors in buck during female natural estrus in their ex situ habitat.


Material A pair of sambar deer (Cervus unicolor Equinus) were

monitored, a doe named Mimi (No. 1, approximately six years of age at the beginning of this study) and a buck named Ujang (No. 2, six years of age) housed at Commercial Zone and Animal Laboratory, Department of Animal Science, Faculty of Agriculture, University of Bengkulu, Indonesia. The deers live together and have free access to the natural photoperiod in an outdoor paddock (5 x 6 m) during the daytime, and they are isolated in individual indoor chambers at night (2 x 3 m). They are sexually mature based on their individual ages during this study was conducted. Doe No.1 was parous before the present study began. They were fed a cut and carry diet consisting of grass, legumes and concentrate daily with proportion of 12 : 2 : 3, respectively. Drinking water was available ad libitum.

Procedures Generally in Indonesia, from August to March is

classified into rainy season and from April to July is classified into dry season (BMKG 2009). Furthermore, in this study the period of June-July 2009 represented dry season while the period of August-September 2009 represented rainy season.

Daily observation of visual estrus manifestations of individual doe and visual sexual behaviors in buck during

female natural estrus was conducted using focal-animal sampling to determine frequent of bout of every manifestation and behavior (She-Jin et al. 2007) by two animal keepers where no specific observation time during 0800 to 1700 h from June to September 2009 (four months). Observations were made outside the paddock from a site of path where the sambar deers were not disturbed.

Doe visual estrus manifestations included apparent reddening and swelling of the external genitalia, loss of appetite and a natural tendency of the doe to approach the buck (Villamor 1985). Each estrus manifestation was scored as one (1) for the presence of the estrus indicators and zero (0) for the absence of the estrus indicators. They were recorded daily during two months of dry and rainy seasons.

Sexual behaviors of the buck were categorized as either actions or states, by using all-occurrence recording method (Webster and Matthews 2006). Sexual behavior included vocalization, flehmen, penile erection (excluding copulation), chasing, mounting, copulation and fighting (Putranto et al. 2005, 2007). The sexual behavior in this study has been used for other male mammals (Schmidt et al. 1988, 1993; Brown et al. 2001) except for fighting behavior.

Data analysis All data are shown as the mean ± standard error of the

mean (SEM). Paired-sample t-test subsequently conducted for each behavior to determine whether the sambar deer’s behavior was influenced by the season (dry and rainy season or not) (She-Jin et al. 2007). The rainy season defined as the month with average rainfall over 100 mm during ten consecutive days. In contrast, the dry season defined as the month with average rainfall below 100 mm during ten consecutive days. Estrous cycle length was calculated as the number of days from the first appearance of apparent reddening and swelling of the external genitalia of one cycle to the appearance of apparent reddening and swelling of the external genitalia in the following cycle (Putranto et al. 2010). Total daily estrus manifestations and sexual behavior scores were expressed as monthly frequency.


In order to preserve sambar deer population in Bengkulu province required a well managed domestication system. Ex-situ conservation located at University of Bengkulu with the deer collection and individual rooms would be a good example for a managed domestication system. The domestication program by conducting an intensive management such as cut and carry system feeding, a monitored sexual activities, a continously health examination and desease prevention including well provided drugs and additive supplements (vitamins) will ensure a daily basic welfare needed for a healthy live of sambar deer. For a long term objectives, these efforts will avoid the preserved species from extinction.


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Sumatran sambar deer is classified as a native ruminant of Bengkulu province, Sumatra – Indonesia. It is well known that in female ruminant, the easiest way to detect the reproductive status is through visual estrus manifestation such as apparent reddening and swelling of the external genitalia (Villamor 1985; Putranto et al. 2010). Individual estrus of a doe was observed monthly throughout this study period. The total average of estrus length and estrous cycle was 2.00 ± 0.41 days (range = 1 – 3 days, n = 8) and 25.00 ± 5.22 days (range = 18 – 37 days, n = 4), respectively (Table 1). Estrus length of doe in this study was last for 24 to 72 hours every 25 days in 4 consecutive cycles. It is agree to a previous study that generally doe is in heat for 24 hours every 28 days for 2 to 3 consecutive cycles (Craven and Hygnstrom 1994), 24 to 48 hours every 20 days in timor deer (Garsetiasih and Takandjandji 2006) and 20 to 25 hours every 17 – 18 days in calamian deer (Villamor 1985).

There were four visual estrus manifestations in this study such as the apparent reddening, swelling of external genitalia, lost of appetite and natural tendency of the doe to approach the buck (Table 2). The apparent reddening and swelling of external genitalia were appeared monthly in dry and rainy season, and the mean and range of those visual estrus manifestations are shown in Table 2. However, season has no effect on the apparent reddening, swelling of the external genitalia and natural tendency of the doe to approach the buck (p > 0.05). Doe significantly lost of appetite during dry season (June – July 2009) than rainy season (August – September 2009) (t = 0.035, p < 0.05). It can be assumed that these signs can be used as indicators for doe reproductive status of Sumatran sambar deer in this study.

Table 1. Individual mean (± SEM) length of estrus and estrous cycle in female Sumatran sambar deer.

Montha) Estrus length (days) Estrous cycle (days) June 2 25 July 2 37 August 2 20 September 2 18 Average 2 25 Note: a) Months in the year of 2009. Table 2. Individual mean (± SEM) frequency of visual estrus manifestations appearances in female Sumatran sambar deer.

Montha) Estrus manifestation appearances Ab) Bc) Cd) De)

June-July (dry) 2.0ns 2.0ns 4.5a 7.5ns August-September (rainy) 2.0ns 2.0ns 0.0b 0.0ns

Note: a) Month in the year of 2009, b) Apparent reddening (number of days per bi-monthly), c) Swelling of external genitalia (number of days per bi-monthly), d) Loss of appetite (times per bi-monthly during female natural estrus), e) Natural tendency to approach the buck (times per bi-monthly during female natural estrus), ns Means in a vertical line differ non-significantly from each other when analyzed by t-test (p > 0.05), a,b Means in a vertical line differ significantly from each other when analyzed by t-test (p < 0.05).

Table 3. Individual mean (± SEM) frequency of visual sexual behavior appearances in male Sumatran sambar deer.

Montha) Sexual behavior appearances

(times in bi-monthly)Eb) Fc) Gd) He) If) Jg) Kh)

June-July (dry) 1.5ns 0.0ns 0.0ns 49.0ns 0.0ns 0.5ns 11.0a August-September (rainy)

7.0ns 16.5ns 4.0ns 111.5ns 2.0ns 2.0ns 46.0b

Note: a) Month in the year of 2009, b) Buck vocalization, c)

Flehmen, d) Penile erection, e) Buck chase the doe, f) Buck mount the doe, g) Copulation, h) Buck fighting, ns Means in a vertical line differ non-significantly from each other when analyzed by t-test (p > 0.05), a,b Means in a vertical line differ significantly from each other when analyzed by t-test (p < 0.05).

One important character of tropical deer is that they can

breed throughout the year or polyestrous (Craven and Hygnstrom 1994; Semiadi et al. 2005). The findings of this study indicated that breeding of Sumatran sambar deer may take place any time of the year. A seasonal factor has a non-significant effect on doe estrus manifestations except for its loss of appetite. According to previous report (BMKG 2009), the average of daily temperature and humidity during dry season in Bengkulu were 26.3℃ and 87%, respectively. Dry-humid condition during dry season influences doe feed consumption. Physiologically during heat-stress, body will reduce feed intake and increase water intake.

A natural tendency of does in approaching to the buck is an indicator for sexual receptivity that accompanies estrus (Villamor 1985). In this study, doe approached the buck in the same day as her visual estrus manifestation (apparent reddening and swelling of the external genitalia) which appeared on date 18-19 June and 26-27 July 2009. The natural tendency to approach the buck which was more frequent in dry season than in rainy season. In contrast, we observed that during rainy season, buck was less aggressive in fighting and had fewer libidos (no penile erection and mounting activity) than in dry season.

The mean and range of visual buck sexual behaviors in dry and rainy seasons are shown in Table 3. A Seasonal factor has no effect on vocalization, flehmen, penile erection, chasing, mounting and copulation (p > 0.05). However, the seasonal factor has a significant effect on fighting behavior with the value of t was 0.036 (p < 0.05). Another mammal such as felids (Putranto et al. 2007), their vocalization and flehmen are probably sexually receptiveness sign. During rainy season, buck vocalization and flehmen were first noticeable and dominant sexual activity in this study. The previous report stated that vocalization and flehmen are visually easy to be seen and detectable breeding behaviors in mammal species (Putranto et al. 2007a; 2008).

During breeding season, the buck aggresiveness increase (Craven and Hygnstorm 1994), and the result showed the increasing buck sexual activities can be seen during rainy season. Those sexual behaviors seem stimulated buck libido as seen by the increasing frequency of buck chasing and fighting activities. In this phase, doe did not show any natural tendency to approach the buck.

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Furthermore, the buck was sexually active which is recorded by his mounting activity, penile erection, and finally by copulation. The main breeding activities such as mount, penile erection and copulation are typically to be appear in September.

Another Indonesian deer species, known as timor deers (C. timorensis) can deliver one or twin offspring in a year (Garsetiasih and Takandjandji 2006). During 2006 to 2009, a pair of Sumatran sambar deer in this study have not been successful in a breeding season as number of offspring produced is n = 1 level. In East Kalimantan preservation, sambar deer conception rate was 30.9% and classified as low (Semiadi et al. 2005). There were 4 copulations recorded during this study. However, the pregnancy of doe in this study until the study accomplished in September 2009, is still unclear.

CONCLUSIONS

It can be concluded that it was possible to assess non-invasively estrous cycle of Sumatran sambar deer by the observation of visual estrus manifestations and there was less of seasonal effect on doe-buck sexual behaviors during female natural estrus in their ex situ habitat.

ACKNOWLEDGEMENT

Authors gratefully acknowledge Professor Osamu Doi and Dr. Satoshi Kusuda of Gifu University Japan for their kind discussion. This project was funded by Directorate General of Higher Education, the Ministry of National Education of the Republic of Indonesia through Fundamental Research Grant (contract number 5006/94/J30.2/PG/2009).

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Muchsinin M, Semiadi G, Dradjat A, Farida WR (2002) Developing sambar deer as new domesticated animal in East Kalimantan. In: Ungulate bioecology and conservation. Bogor, Indonesia. [Indonesian]

Mukhtar AS, Suita E (2002) Market demand for venison in Jakarta restaurants. PS Ilmu Hayati IPB, Bogor. [Indonesian]

Putranto HD, Kusuda S, Doi O (2005) The compatability between musth and estrus in the reproductive cycle of Asiatic elephants by noninvasive measurement. In: Indonesian student meeting. Nagoya University, Japan, 1-2 September 2005.

Putranto HD, Kusuda S, Ito T, Terada M, Inagaki K, Doi O (2007) Reproductive cyclicity based on fecal steroid hormones and behaviors in Sumatran tigers, Panthera tigris sumatrae. Jpn J Zoo Wildlife Med 12(2): 111-115.

Putranto HD, Soetrisno E, Nurmeiliasari (2008) Reproductive physiology of sambar deer (Cervus unicolor Equinus), Bengkulu endemic ruminant. LPPM Universitas Bengkulu, Indonesia. [Indonesian]

Putranto HD, Soetrisno E, Nurmeiliasari (2010) Monthly live weight gain and estrous cycle estimation of domesticated female sambar deer. In: Widiyono (ed) Revitalisasi program studi dan peningkatan peran perguruan tinggi ilmu-ilmu pertanian. Universitas Bengkulu, Bengkulu, 23-25 May 2010. [Indonesian]

Semiadi G (2002) Tropical and non-tropical deer farming potency. Ps Ilmu Hayati IPB, Bogor. [Indonesian]

Semiadi G, Muir PD, Barry TN, Veltman CJ, Hodgson J (1993) Grazing pattern of sambar deer (Cervus unicolor) and red deer (Cervus elaphus) in captivity. New Zealand J Agric Res 36: 253-260.

Semiadi G, Muir PD, Barry TN (1994) General biology of sambar deer (Cervus unicolor) in captivity. New Zealand J Agric Res 37: 79-85.

Semiadi G, Nugraha RTP (2004) Tropical deer management. LIPI, Bogor. [Indonesian]

Semiadi G, Adhi IGMJ, Trasodiharto A (2005) Calving pattern of captive sambar deer (Cervus unicolor) in East Kalimantan. Biodiversitas 6 (1): 59-62.

Soetrisno E, Putranto HD, Nurmeiliasari (2009) Reproductive physiology of sambar deer (Cervus unicolor Equinus), Bengkulu endemic ruminant. LPPM Universitas Bengkulu, Indonesia. [Indonesian]

She-Jin L, Lin Y, Yu-qing L, Yan Y, Guo-Hong C, Wan-Hong W (2007) The effect of visitor density on the behavior of the captive fallow deer (Dama dama). Res J Anim Sci 1(3): 81-84.

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Schmidt AM, Hess DL, Schmidt MJ, Lewis CR (1993) Serum concentrations of oestradiol and progesterone and frequency of sexual behaviour during the normal estrous cycle in the snow leopard (Panthera uncia). J Reprod Fertil 98: 91-95.

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Demersal fishes and their distribution in estuarine waters of Mahakam Delta, East Kalimantan

IWAN SUYATNA1,♥, ACHMAD ARIFFIEN BRATAWINATA2, ACHMAD SYAFEI SIDIK1, AFIF RUCHAEMI2 1Faculty of Fisheries and Marine Science, Mulawarman University (UNMUL). Jl. Gunung Tabur, Kampus Gunung Kelua, Samarinda 75116, Kalimantan

Timur, Indonesia. Tel./Fax.: 0541-748648; 081347935111; ♥email: [email protected] 2Faculty of Forestry, Mulawarman University (UNMUL), Samarinda 75116, Kalimantan Timur, Indonesia.

Manuscript received: 9 April 2010. Revision accepted: 23 August 2010.

ABSTRACT

Suyatna I, Bratawinata AA, Sidik AS, Ruchaemi A (2011) Demersal fishes and their distribution in estuarine waters of Mahakam Delta, East Kalimantan. Biodiversitas 12: 204-210. The study aimed (i) to identify of the demersal fishes, (ii) to analyze the diversity and (iii) to determine their distribution. Surveys were carried out between August 2009 and January 2010 in Mahakam Delta, East Kalimantan. Data were analyzed using several indices of Shannon Weaver, Sympson, Margalef species richness, and Bray Curtis distance. The canonical correspondence analysis (CCA) was also used to correlate between fish species and their environmental factors and to show the fish distribution. Sixty samplings were done using bottom-trawl at various water depths from one to fourty two meters to collect the data. Taxonomically, during the study, 10 orders, 61 families, 87 genera and 131 species of fish with 43340 individuals were identified. Among the families, Leiognathidae was the most important group of fish, they distributed throughout the depths. Meanwhile CCA showed that Leiognathidae and Sciaenidae were observed to be rich in the shallow water. Generally, index of Shannon Weaver, Sympson and Margalef species richness ranged between; 0.52 and 2.48; 0.11 and 0.82; 2.24 and 18.61 respectively. Bray Curtis distance indicated the significant difference of individual number of demersal fishes between shallow and deep waters.

Key words: Mahakam delta, water depth, trawl, demersal fish, canonical correspondence analysis.

INTRODUCTION

The Mahakam Delta is located on the East of Kalimantan between S 0o21’ and 1o10’, and E 117o15’ and 117o40’ (Sandjatmiko, 2006). Due to its 1500 km2 of mangroves and channels, the Mahakam Delta is a place that is not easy to reach (Dutrieux, 2001), then Madeo (2001) stated that starting from 1990’s the development of aquaculture has changed the environment up to 76% as a global human impact. Mangrove area conversion into shrimp pond tambak is the major factor. The thickness of the green belt was only ranging from 30 to 193 m (Suyatna et al., 2010). Kamal (2006) estimated Mangrove destruction 30% of 6273.5 ha caused a decrease of fish catch of about 975.0 tons year-1. While ongoing mangrove degradation, the Mahakam Delta has also been significantly pertubed by trawl fishing in the past 25 years because the Presidential Decree no 39 year 1980 acts to forbid the operation of trawls in Indonesia, the trawls are still operated in the delta up to present. According to Remesan and Ramahandran (2005) mini trawls are usually operated in the sea by the artisanal fishermen and based on the target group, three types of trawls are in operation namely fish, shrimp and crab trawl. Can (2006) identified that the trawls are not very selective and catches are composed of a highly diversified mix of fish. While Firdaus (2010) described the catch between trawls and trap nets is significantly different, the first could fished 16.10 kg/h and others only 1.67 kg/h. Budiman et al. (2006) had reported that an overfishing of

the demersal fish was occured in Kendal waters of Kendal district. Results of the above study were among the reasons why the study related to biological aspects in Mahakam Delta is needed to be performed. The study aimed (i) to identify of the demersal fishes, (ii) to analyze the diversity and (iii) to determine their distribution.


The study was carried out between August 2009 and January 2010 in Mahakam Delta, East Kalimantan. Sampling areas were divided into three strata on the basis of depth: Stratum I or shallow: 1 to <10 m; Stratum II or intermediate: <10 to <20 m and Stratum III or deep: 20 to 42 m. A total of 60 bottom trawl hauls consisting of 20 hauls for each stratum (shallow, intermeditate and deep) were performed using a motorized boat sizing 12m x 2m x 1.5m and equipped with a net size of 10 m length. The hauls were considered as sampling sites (observations). Double machines were used at the intermediate and deep sampling areas to increase the power of the boat. Towing time varied from 15 to 25 minutes. Garmin GPSMap 60CSx recorded the geographic positon of all sites. Fish identification referred to the field guide book of Peristiwady (2006), Allen (2000), and Masuda et al. (1975). The physico-chemical properties of waters were measured in situ at the sea surface using water checker Horiba, except water transparency. All data of fish

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including environmental factors were analyzed using statistical software. Index of Shannon-Weaver, Sympson, Margalef species richness (using log) and the canonical correspondence analysis (CCA) except the Bray Curtis distance were made by statistical program of the Brodgar version 2.6.5. The Bray Curtis distance was analyzed by using software of the PAlaeontological STatistics, PAST version 2.0. Graphs of the CCA was realized by the Brodgar, map of Mahakam Delta by MapINFO 8.5 while others were made by hand.


The general conditions of the study area (south, center and north part) related to the distribution of geographic position of the sampling sites, the distance of each sampling site from the coastline, and the bathimetry are presented in the Figure 1. Taxonomically, our study identified the main fish orders as presented in the Table 1. The measurement result of the physico-chemical properties and the environmental factors are summarized as shown in the Table 2. Table 1 shows that only the concentration of turbidity did not follow general condition. The turbidity should be less as more away from the coast, but it is possible to accept this condition as being valid because the turbid water of the big River of Mahakam highly affected the sea. Such environmental factors were studied in order to observe their effects on the demersal fish distribution as Moyle and Cech (2000) stated that the distribution and abundance of fish found out in estuaries are determined primarily by physical and chemical factors and only secondarily by biological factors.

Fish community structure During the study, 10 orders, 61 families, 87 genera and

131 species of fish with 43340 individuals were identified and listed in the table below. From those data, the structure of fish community in the Mahakam Delta was revealed as presented in the Table 3.

Navaro et al. (2010) only could collect 64 demersal fishes from 36 fish families in the eastern coast of the mouth of the gulf of California during eight surveys aboard a commercial shrimp trawling boat that operated at the depth of 10 to 60 m during the 2005/06 and 2006/07 shrimp fishing seasons. Budiman et al. (2006) in their study on the distribution analysis of demersal fishes in Kendal found out 44 families and the most number of the species belonged to Apogonidae. Related to the fish community structure, our study showed that 87% of 60 obsevations the fish diversity index varied between 1 and 2.09 belonging to the intermediate level, and the index of less than one and more than three belongs to the category Low and High. Ridho and Suman (2003) studied the relationship between fish community structure and biomass of demersal fishes in various water depths. They found out that the fish diversity was much more stable in water depth of ≤ 30 m and showing the higher the fish diversity index the greater the fish biomass. We found out the similar result with that finding. Individual number of fish of our study showed that

the shallow water was higher than deep waters as well as the fish diversity (Figure 2 and 3). Budiman et al. (2006) found out less fish population at depth ≥ 10 m, and the same finding was also observed in the Mahakam Delta. Higher Sympson index (C) was identified in the shallow water and this means that there was one or more species extremely high in population (dominant), where the index closes to one means that there was dominant species, the criterion index is 0 ≤ C < 0.5 low dominance, 0.5 ≤ C < 0.75 intermediate dominance and 0.75 ≤ C < 1.0 high dominance. Ponyfish or Pepetek belonging to the family Leiognathidae (its member presented in Table 5) were the most populated with total number of 15860 individuals (36.59%). While other dominance demersal fish species was represented by Croakers or Gulamah (Johnius amblycephalus, Bleeker 1855 and Atrobucca brevis Sasaki and Kailola 1988) belonging to the family Sciaenidae and Longfin Anchovy or Bulu Ayam/Bilis (Setipinna tenuifilis, Valenciennes 1848 and Thryssa mystax Bloch and Schneider 1801) belonging to the family Engraulidae with their individual number were 7310.0 (16.86%) and 7520.0 (17.35%) respectevely. Totally, individual numbers of fish of each stratum from shallow to deep were 24216, 7250 and 11874 individuals respectively. The diversity index in our study (Table 3) was higher compared to the index reported by Genisa (2006) who studied in the Mahakam Delta that ranged from 0.53 to 1.55. However Margalef species richness was much lower compared to 13.18 to 23.70. This might prompt a drop in abundance in the Mahakam Delta at present like that occured in the Gulf of Thailand. In the Gulf the abundance of Leiognathus had dropped from 27.4% to 7.6% in ten years caused of the heavy trawl fishing (Longhurst and Pauly 1987).

Margalef species richness in shallow waters of the Mahakam Delta was higher compared to the intermediate and deep waters as well (Figure 3) but not significantly different. More detail of explanation related to the individual and fish species number difference among the strata, statistically it could be seen in the Tabel 4. According to the analysis of Bray Curtis distance, the individual number of fish in the shallow compared to the intermediate and deep waters showed significantly different but not between the intermediate and the deep waters. However, the fish species number was almost all similar. The value of the Bray Curtis distance closes to one means that the two objects are more similar.

Table 1. Orders of the demersal fish species identified during the study within the Mahakam Delta.

Order No of family

No of genus

No of species

Perciformes 37 54 95 Tetraodontiformes 4 8 8 Scorpaeniformes 4 3 6 Clupeiformes 3 9 9 Pleuronectiformes 3 3 3 Rajiformes 3 3 3 Syngnathiformes 2 2 2 Siluriformes 2 2 2 Anguilliformes 1 1 1 Aulopiformes 1 1 1 61 87 131

BIODIVERSITAS 11 (4): 204-210, October 2010 206

Tabel 2. The summarized measurement result of the environmental factors related to the condition of the study area during the study in the Mahakam Delta.

Sampling areas

Distance (km)

Depth (m)

Salinity (g/L)

Turbidity (mg/L)

Transp. (m)

DO (mg/L)

Shallow 0.03-9.60 1.00-9.10 3.10-31.00 1.00-173.00 0,40-2.30 3.40-7.20Intermediate 0.07-18.0 10.0-18.0 2.10-34.80 3.00-198.00 1.00-7.00 4.00-6.00Deep 4.60-16.90 22.5-42.0 25.40-34.60 1.00-336.00 1.00-8.70 3.00-6.80 Table 3. The diversity indices of the fish community structure based on the water depth strata during the study in the Mahakam Delta.

Diversity Water depth strata Index category Shallow Intermediate Deep

Shannon Weaver Hln 0.13 to 2.09 0.26 to 2.08 0.30 to 1.98 1 and >3 Sympson C 0.18 to 0.96 0.14 to 0.91 0.17 to 0.89 0 and1 Margalef R 4.46 to 17.58 2.24 to 16.68 3.48 to 15.71 - Range no of individual 71.00 to 6242.00 16.00 to 1452.00 88.00 to 3042.00 = 43340 ind Range no of species 5.00 to 18.00 3.00 to 18.00 5.00 to 17.00 = 131 species

Figure 1. Map showing the distribution of sampling sites (left) and overlapped with the bathimetry and the deltaic plain (right) of the Mahakam Delta of East Kalimantan.

Figure 2. Individual number of fish of the three strata (shallow, intermediate and deep waters) during the study in the Mahakam Delta.

Figure 3. The index of Margalef species richness of the three strata during the study in the Mahakam Delta.

In the Table 5, we presented four families which comprising the most number of species in their groups identified in the Mahakam Delta in order to show the comparison of the body size between permanently and non permanently demersal fish from part of our samples.

The majority of ponyfish were observed living throughout the observed sites, very small body size and much smaller compared to other groups. Only L equulus the length and weight could reach more than 20 cm and 100 g Several members of those fishes of our samples can be seen below (Figure 4).

In Irian Jaya, Genisa (2001) found out that the most important and populated estuarine demersal fish were family Haemulidae. In 2003 he continued to study on the distribution and fish community structure in the same place, but he just found out four species of ponyfish L splendens, L brevirostris, L fasciatus and S ruconius (Genisa, 2003). Only L brevirostris Valenciennes 1835 was not identified. A study of ponyfishes composition in West Sumatera found out 10 species of Leiognathus and one species each from the genera of Secutor and Gazza (Wedjatmiko, 2007). . In the Mahakam Delta, the fishes were identified 11 species, almost half of the total number of species living in the Indonesian Waters. Therefore, up to this point we conclude that the Mahakam Delta is rich in fish species because not only homed many its own fish species but also nurses varied fish species from other environments. Although in small number and relatively small size compared to their real size, we found out many species from outside of the Mahakam Delta as presented in the Table 5. This has a relation with the statement of Svedang (2003) that the inshore demersal fish community were dominated by immature fish that disappear when they grow older and most likely migrate offshore.


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Table 4. Similarity of individual and species number between two strata based on the Bray Curtis distance during the study in the Mahakam Delta.

Based on the individual number Based on the species number Strata Shallow Intermed. Deep Strata Shallow Intermed. Deep

Shallow 1 0,46081 0,65802 Shallow 1 0,93249 0,97778 Intermed. 0,46081 1 0,75821 Intermed. 0,93249 1 0,95464 Deep 0,65802 0,75821 1 Deep 0,97778 0,95464 1

Table 5. The demersal fish species and their size distribution identified during the study within the Mahakam Delta.

Estuary Lenght weight distribution

Sample Lenght (cm) Weight (g) Size Min Max Min Max

Ponyfishes (Leiognathidae)

Leiognathus equulus (Forsskal 1775) 3453 3.5 20.5 0.81 120 L. fasciatus (Lacepede 1803) 1 13 13.5 42.3 43 L. splendens (Cuvier 1829) 3278 2.5 17 0.35 74 L. leuciscus (Gunther 1840) 560 5 12 0.9 27.14 L. bindus (Valenciennes 1835) 1909 3.5 11.6 0.62 23.5 L. nuchalis (Temminc and Sckege l845) 24 7.5 10 5.6 14.2 L. elongatus (Gunther 1874) 62 10.2 14.2 16.9 41.6 Gazza minuta (Bloch 1797) 1484 4 13 0,51 27 G. achlamys (Jordan and starks 1917) 2592 8.3 14 9.2 42 Secutor ruconius (Hamilton 1822) 2492 3.5 11 0.7 17 S. indicius (Monkolprasit 1973) 5 8 10.8 5 16.3

Marine Trevallies (Carangidae) Caranx sexfasciatus (Quoy and Gaimard 1825) 15 9 24 9.43 160 Carangoides dinema (Bleeker 1851) 16 13.5 25 33 260 C. talamparoids (Bleeker 1852) 19 9.5 20 11.5 129 C. ferdau (Forsskal 1775) 8 10.5 16 15.11 58.14 C. uii (Wakiya 1924) 13 10.5 14 17.06 38.9 C. hedlamdensis (Whitely 1934) 16 14.5 25 34.5 240 C. chrysophrys (Cuvier 1833) 3 25 25 260 260 Psenopsis humerosa (Munro 1958) 2 10 12.5 19 33 Gnathanodon speciosus (Forsskal 1775) 4 6,5 14 4 38 Ulua mentalis (Cuvier 1833) 37 6 24 5 240 Alectes ciliaris (Bloch 1788) 3 4 25 2.2 240 A. indicus (Ruppell 1828) 7 6 29 3.4 390 Groupers (Serranidae) Epinephelus merra (Bloch 1793) 2 20 20 100 162.38 E. coioides (Hamilton 1822) 7 11 40 15.65 1000 E. amblycephalus (Bleeker 1857) 9 15 26 20 240 E. sexfasciatus (Valenciennes 1828) 2 9 16 9 215 E. ongus (Bloch 1790) 1 18 - 83 - Cephalopholis microprion (Bleeker 1852) 1 17 - 80 - C. formosa (Shaw and Nodder 1812) 1 16 - 134 - Snappers (Lutjanidae) Lutjanus erythropterus (Bloch 1790) 2 9 29 12,15 360 L. johnii (Bloch 1792) 30 7 75 4.64 5300 L. ruselli (Bleeker 1849) 31 7 19,5 12.5 280 L. quinquelineatus (Bloch 1790) 1 13.5 - 15 - L. vitta (Quoy and Gaimard 1824) 1 14 - 28.4 - L. lutjanus (Bloch 1790) 90 8 15,5 5.5 45 L. malabaricus (Bloch and Schneider 1801) 15 12.5 35 27.9 740

To give an idea the demersal fish species came from the marine environment from among of our samples, please refer to Figure 5, 6 and 7.

Fish distribution English (1994) suggested that

to study fish distribution, observe the correlation between fish species and the environmental factors, and this would be helpful. In relation to this, the study used the CCA that could analyze the combination of three variables (species, environmental factor and site) and show the correlation. Many authors used the this tool such as Sanchez and Serrano (2003) and Byron and Link (2010). From the correlations, the distribution pattern of fish could be viewed easily. The result of the CCA of our study showed that the environmental factors (bold lines) except the dissolved oxygen (DO), namely transparency, salinity, depth, distance and turbidity denoted by Trans, Sali, Depth, Dist and Turb had highly correlation between each other (Figure 11).

On the figure, salinity and depth were sticked together, H42 is showing a site with depth of 42 m. Again, through viewing on the triplot and biplot of the CCA, we can simply interpret the major distribution of demersal fishes. The CCA shows that Cardinalfish or Gelageh (such as Apogon kiensis Jordan and Snyder 1901 and A poecilopterus Cuvier 1828) denoted by (Gelg) belonging to Apogonidae, Herrings or Selangat (Anodontostoma chacunda Hamilton 1822 and Hilsa Keele Cuvier 1829) denoted by (Slngt), Puput or Ditchelee (Pellona ditchela Valenciennes 1847) denoted by (Pupt) belonging to Clupeidae, Croakers or Gulamah (Johnius amblycephalus and Atrobucca brevis) denoted by (Gul) belonging to Sciaenidae, Longfin Anchovy or Bulu Ayam (Setipinna tenuifilis and Anchovy or Bilis (Thryssa mystax) denoted by (BulA) and (Bils) belonging to Engraulidae, Sailfin Perchlet or


Table 6. Distribution of species on the basis of fish group and water depth in the Mahakam Delta.

Common name Local name No of species

Water depth Species category Shallow Inter-

mediate Deep

Ponyfishes Pepetek 10 √ √ √ Demersal fishGoatfishes Niko 2 √ √ √ Demersal fishSylver biddies Kapas-kapas 4 √ √ √ Demersal fishSnappers Kakap 7 √ √ √ Demersal fishTrevallies Ikan Putih 12 √ √ √ Demersal fishGroupers Kerapu 8 √ √ √ Demersal fishKingfish Baji-baji 1 √ Demersal fishBlack kingfish Gabus laut 1 √ Demersal fishMoonfish Terang bulan 1 √ Demersal fishFlutemouth Ikan terompet 1 √ Demersal fishBigeye Mata besar 1 √ Demersal fish 48

Beseng (Ambasis interuptus Bleeker 1852) denoted by (Bsng) belonging to Chandidae; all those species negatively correlated with the environmental factors including sites (water depth). The Croakers and Anchovy, according to Moyle and Cech (2000), are often found as inhabitants of turbid estuaries, bays and rivers, and the distribution and the abundance of fish found in estuaries are mainly determined by physical and chemical factors. We might conclude that the

Figure 4. Members of the Family Leiognathidae (From left L equulus, L splendens, L nuchalis, G minuta and S ruconius (Source: Original photos taken from the samples).

Figure 5. Members of the Family Lutjanidae (From left Lutjanus decussatus, L malabaricus, L russeli, L quinquelineatus and L erythropterus. (Source: Original photos taken from the samples).

Figure 6. Members of the Family Carangidae (From left Carangoides dinema, C. hedlamdensis, Gnathanodon specious, C. talamparoids, Ulua mentalis. (Source: Original photos taken from the samples).

Figure 7. Members of the Family Serranidae (From left Epinephelus coioides, E sexfasciatus, E merra, E ongus dan Cephalopolis formosa (Source: Original photos taken from the samples).

Figure 9. Members of the Family Sciaenida and Engraulidae (From left Atrobucca brevis Sasaki and Kailola 1988, Johnius amblycephalus Bleeker 1855, Thryssa mystax Bloch and Schneider 1801 and Setipinna tenuifilis valenciennes 1848.

Figure 10. Members of the Family Rachycentridae, Carangidae, Priacanthidae and Menidae (From left Rachycentron canadus Linnaeus 1766, Seriola fasciata Bloch 1793, Priacanthus tayenus Richardson 1846 and Mene maculata Bloch and Schneider 1801.


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H6H5

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Figure 11. Triplot (left) and biplot (right) of the CCA showing correlation among species, environmental factors and sites (denoted by H) and between species and sites. mentioned fish groups were strictly living in shallow water near the coastline from 30 m up to 9600 m and their distribution was limited mainly by the environmental factors of salinity and water depth. Ecologically, Pepetek or ponyfish members of the family Leiognathidae such as L equulus, L splendes G minuta, S. ruconius and others denoted by (Petek) mainly inhabit the same environment but because some of these species distributed up to the sea (deeper, denoted by H and the number beside the letter showing water depth), thus they (Petek) separated from (Gelg), (BulA), (Bils) and (Gul). Navarro et al. (2010) surveyed at depth 10 to 60 m, the family with the most species was Sciaenidae. Several of our samples related to those fishes are shown in the Figure 9 above.

Other species such as Mata Besar or Bigeye Priacanthus sp, Baji-baji or Kingfish Seriola sp, Gabus Laut or Cobia Rachycentron sp, Terang Bulan or Moonfish Mene sp (please refer to Figure 10 for the complete species names and their authors), ikan Terompet or Flutemouth Fistularia petimba Lacepede 1803 denoted by (Matp), ikan Niko or Goatfishes Upeneus sp denoted by (Niko) and Kape-kape or Sylver biddies Gerres sp denoted by (Kape) positively correlated with the environmental factors. In other words, they prefer to inhabit very saline and tranparent water away from the coastline up to more than 16000 m. These fish groups were strictly living in deeper water and their distribution are limited at least by the environmental factors of salinity, water turbidity, water depth and DO concentration. In connection with the demersal fish distribution, probably other environmental factors might also play an important role as Parry et al. (1995) in their study on the distribution, abundance and diets of demersal fish at depth 07 m (shallow waters), 12 to 17 m (intermediate waters) and 22 m (deep waters). The demersal fish distribution is linked to the spread of foods and preys and sedimentary types as well.

From a total of 131 species, 43 species formed six groups and to exhibit a wide range of distribution within the study area, and five species were restricted to the deep water (Table 6).

CONCLUSION

During the study, in the bottom trawls, 131 demersal fish species belonging to 87 genera, 61 families and 10 orders were identified. The most abundant fish was Pepetek or Ponyfishes (15860 individuals, 36.59%) and they distributed throughout the observed sites from shallow to deep as well as from brackish to salt waters, Bulu Ayam or Longfin Anchovy (7520.0 indiviuals, 17.35%) and Gulamah or Croakers (7310.0 individuals, 16.86%). Based on the CCA, Herrings, Croaker, Longfin anchovy, Anchovy, Ditchelee, Cardinalfish and Sailfin perchlet had strongly negative correlation with salinity, distance, water depth, turbidity and transparency. Meanwhile Black Kingfish (Cobia), Bigeye, Goatfish, Threadfin bream, Sylver biddy, Flutemouth and Moonfish were strongly and positively correlated with the environmental factors. Thus, members of the first family groups were distributed approaching the coastline, while the second ones tended to be away from the coastline.

ACKNOWLEDGEMENTS

We would like to thank Dean Faculty of Fisheries and Marine Science Mulawarman University, Marine Affairs and Fisheries Service of Tenggarong and TotalFina E&P Balikpapan for the collaborative works.


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Diversity of some fauna in National Chambal Sanctuary in Madhya Pradesh, India

PREMANAND KALKRISHANA MESHRAM ♥

Forest Entomology Division, Tropical Forest Research Institute, P.O. RFRC, Mandla Rd, Jabalpur- 482021, Madhya Pradesh, India. Tel. +91-761-2840483, Fax. +91-761-2840484. ♥email [email protected]

Manuscript received: 16 August 2010. Revision accepted: 29 October 2010.

ABSTRACT

Meshram PM (2010) Diversity of some fauna in National Chambal Sanctuary in Madhya Pradesh, India. Biodiversitas 11: 211-215. National Chambal Sanctuary (NCS) gives very good account of avifauna. It over emphasizes significant and important birds species available which are of National and International importance. Crocodiles use sand banks for nesting and basking. Fauna in the NCS is very much influenced by various factors like habitat suitability and protection of their habitats. Their distribution is depending on availability of deep water pools. Another important factors on which distribution of animals depends long stretches of long sand banks. Sloppy to steep sand bank with loose soil were good habitats for nesting of crocodiles, turtles and birds. NCS areas were considerably altered and there were disturbance by the sand miners, poachers, fishermen and farmers. Consequently the poor survival is recommended to greater protection by management practices. Effective co-operations between the Forest Department of Madhya Pradesh and neighbouring states were needed as sand mining and poaching becomes an interstate problem. Thus, strategic location of this site in the migratory route of water birds enhances its importance as a significant water bird habitat. In the present study diversity of some fauna in NCS is discussed.

Key words: national chambal sanctuary, fauna, diversity.

INTRODUCTION

In India, National Chambal Sanctuary is lying in three states of Madhya Pradesh, Uttar Pradesh and Rajasthan. The interstate boundary of Madhya Pradesh and Rajasthan along the Parvati river up to the point where Chambal right main canal crosses the Parvati river and the interstate boundary of Madhya Pradesh, Rajasthan and Uttar Pradesh running parallel at a distance of one km either side of Chambal river has been declared National Chambal Sanctuary for Crocodile (Crocodylus palustris), Gharial (Gavialis gangeticus) and other wild animals. During 1978 the Chambal river was declared as a Crocodile Sanctuary under Crocodile Project with an aim to provide fully protected habitat for conservation and propagation of gharial, crocodilian and other wild animals. The river Chambal is one of the country's most beautiful and least polluted river systems. The National Chambal Sanctuary extends over the Chambal River from Jawahar Sagar Dam to Kota barrage and after a gap of 18 km free zone, from Keshoraipatan (Rajasthan) through Pali to Pachanada Uttar Pradesh where it forms a common confluence with the Yamuna along with the Kunwari, Pahuj and Sindh rivers. The total length of the river inside the sanctuary is about 600 kms. The width of the river that is included inside the Sanctuary is 1000 m from midstream on either side of the bank in Rajasthan and Madhya Pradesh. Uttar Pradesh has a greater width to an area 635 sq. km geographically. The

sanctuary lies between the latitudes 25o 35' N and 26o 52' N and longitudes 76o 28' E and 79o 01' E.

In Madhya Pradesh the Sanctuary runs for a length 435 km. The National Chambal Sanctuary was established to protect this pristine river ecosystem, complete with its varied flora, acquatic life and avifauna. The river harbours a variety of aquatic life like the elusive Ganges River Dolphin (Platanista gangetica), Gharial (Gavialis gangeticus), Crocodile (Crocodylus palustris), seven species of fresh water turtles (Asperidetes gangeticus, Lissemys punctata, Chitra indica, Batagur kachuga, Kachuga dhongoka, Pangshura tentoria and Hardella thurjii), the Otter (Lutra perspicillata) and a variety of fishes. The rare Ganges river Dolphin P. gangetica, the sole member of the cetaceans group is one of the main attractions of the sanctuary. So called the queen of Chambal, the Dolphin inspire of being blind can be seen perusing their playful antics in the water while coming out to breathe for air. The Chambal Sanctuary is one of their safest breeding areas. As per the management plan of National Chambal Sanctuary, around 170 species of birds have been identified in the Sanctuary. Among the different species of birds found in the sanctuary are: bare headed goose, brahmini duck, teals, cormorants, egrets, black and white ibises, brown headed gulls, pointed stork, common crane, sarus crane, herons, spoon bills, pelicans, etc. One can have an easy sighting of the Indian Skimmer- the highest population of which in the world is found in the


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NCS. The other important terrestrial animals present in the ravines of the sanctuary are land monitor lizard, variety of other lizards and snakes, sambhar, porcupine, hares, desert cat, blue bull, wild boars etc. (Anon. 2003). In the present study diversity of some aquatic, terrestrial fauna and their probable impact in National Chambal Sanctuary are discussed.

MATERIAL AND METHODS

The information of general habitat of animals was collected. Habitat analysis was carried out on the basis of river bank types located in different zones both aquatic and terrestrial and the water depth during different seasons. Habitats used by the various animals were observed. Data sheets were prepared to record field observations, interview results, past records etc. A detailed survey was carried out by motorboat and also walking along the river bank. During 5th May, 2010 a stretch of 1.0 km on National Chambal Gharial Sanctuary (Figure 1) was surveyed for

recording the fauna. The fauna is divided into terrestrial and aquatic and exhibits a wide diversity in faunal composition. The aquatic birds were observed with the help of field binoculars. The fauna were identified with the help of Dr. R.K. Sharma, Range Officer, National Chambal Sanctuary, Deori, Morena, M.P. (India) and using management plan of National Chambal Sanctuary (2003).

As a measure of α- diversity (diversity within habitat), the most popular and widely used the following Shannon's diversity index (H') was calculated since it is well accepted that all species at a site, within and across systematic groups contribute equally to its biodiversity (Ganeshaiah et al. 1997).

Shannon's index H' = Σ (pilnpi)

i=1 p= is the proportional abundance of the i th species s =total number of species ln = is the log with base'e' (Natural log)

Figure 1. National Chambral Sanctuary in three states of Madhya Pradesh, Uttar Pradesh and Rajasthan, India (circle).

MADHYA PRADESH

UTTAR PRADESH

RAJASTHAN

Morena

MAP OF INDIA

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Table 2. Density percentage and Shannon diversity index of some aquatic and terrestrial fauna in NCS during 2010.

Scientific name Common name %Density

Dicrurus adsimilis Black drongo 0.766284Vanellus indicus Redwattled lapwing 5.747126Phalacrocorax niger Little cormorant 0.766284Vanellus spinosus Spurwinged plover 1.915709Rynchops albicollis Indian skimmer * 0.766284Hirundo rustica Common swallow 9.961686Merops orientalis Green bea eater 0.766284Dendrocygna javanica Whistling teals 10.72797Egretta garzetta Little egret 0.383142Columba livia Blue rock pigeon 0.383142Acridotheres gingianus Bank myna 1.532567Streptopelia tranquebatica Red tuttle dove 1.149425Burhinus oedicnemus Stone curlew 0.383142Lanius excubitor Grey shrike 45.97701Sterna aurantia River tern 0.766284Strptopelia decaocto Ring dove 0.766284Pavo cristatus Common peafowl 0.766284Neophron percnopterus Scavenger vulture 0.383142Danus chrysipus Plain tiger 1.149425Terias (Eurema) blanda Grass yellow 0.766284Catopsilia crocale Common emigrant 0.766284Orthetrum pruinosum neglectum Dragonfly 1.915709O. taeniolatum Dragonfly 1.149425Gavialis gangeticus Gharial 1.915709Crocodylus palustris Mugger 0.383142Kachuga kachuga Hard shell tuttle 0.766284Labeo rohita Rohu 1.915709Catla catla Catla 0.766284Heteropneustes fossilis Cat fish 4.597701 100Shannon Diversity Index 2.17057


The numbers of fauna sighted, density percentage and Shannon diversity index of some fauna in National Chambal Sanctuary (NCS) during the present study are shown in Table 1 and 2. During the survey the wetland avifauna was observed in higher numbers as compared to other fauna. The surveyed stretch of the site is mainly sandy banks. The sandy banks of river are used by the gharial, mugger and turtle for basking and nesting. Fishes constitute secondary level of food chain. Availability of avifauna in their numbers and available species is another important significant biodiversity criteria that requires immediate attention in this site. World famous Keoladeo Ghana Bird Sanctuary at Bharatpur is only 95 kms away from this site and it is very natural to expect richness species, numbers and offering an extensive habitat for resident as well as migratory birds. Chambal River lies on the migratory route of aquatic fauna providing an approximate stretch of 300 km of perennial wetland habitat for wintering aquatic bird fauna. Most of the entire avifauna recorded in this site are either residents or migrants.

On the basis of data of avifauna clearly indicates that major congregator birds are fish feeders exemplifying the richness of fishes in the river system. This also signifies high levels of primary production in the site. It was also observed that bird population fluctuate in Chambal river which has some direct relation with the habitat condition with Bharatpur which is one of the major habitat for water bird situated 95 km away from this site. It is presumed that during the drought period in Bharatpur more birds take refuse in Chambal River which perhaps includes endangered Siberian Crane which is also reported from Madhya Pradesh. Wetlands are highly productive systems. They are rated third among the highly productive systems of the world. The food chain and food pyramid of NCS is depicted in the following diagram (Figure 2).

In NCS, cattails, Typha spp. is the main aquatic plant. Typha accounts for high level annual net primary production levels (tons/h), which is 10-94 tons/ha. Like primary production the secondary production is also fairly high in wetlands. The secondary production depends upon the pathway and efficiency of utilization of energy in primary production. In wetlands a relatively small portion of primary production of algae and higher plants is directly utilized by herbivores. Large part of plant production is used only after it is dead and partly decomposed. Various benthic organisms, some fishes and dolphins feed on detritus in different stages of decay. Other carnivores

Table 1. Census of some aquatic and terrestrial fauna in NCS during 2010.

Scientific name Common name Family No. of fauna

sightedRemark

Birds Acridotheres gingianus Bank myna Sturnidae 4Burhinus oedicnemus Stone curlew Burhinidae 1Columba livia Blue rock pigeon Columbidae 1Dendrocygna javanica Whistling teals Anatidae 28Dicrurus adsimilis Black drongo Dicrurudae 2Egretta garzetta Little Egret Ardeidae 1Hirundo rustica Common swallow Hirundinidae 26Lanius excubitor Grey shrike Laniidae 120Merops orientalis Green bea eater Meropidae 2Neophron percnopterus Scavenger vulture Accipitridae 1Pavo cristatus Common peafowl Phasianidae 2Phalacrocorax niger Little cormorant Phalacrocoracidae 2Rynchops albicollis Indian skimmer * Laridae 2Sterna aurantia River tern Laridae 2Streptopelia tranquebatica Red Tuttle Dove Columbidae 3Strptopelia decaocto Ring dove Columbidae 2Vanellus indicus Redwattled lapwing Charadiidae 15Vanellus spinosus Spurwinged plover Charadiidae 5Entomofauna

I. Lepidoptera

Catopsilia crocale Common emigrant Pieridae 2Danus chrysipus Plain Tiger Danaidae 3Terias (Eurema) blanda Grass Yellow Pieridae 2

II. Odonata Orthetrum pruinosum neglectum Dragonfly Libellulidae 5O. taeniolatum Dragonfly Libellulidae 3Crocodiles Gavialis gangeticus Gharial Crocodilidae 5 5 nestsCrocodylus palustris Mugger Crocodilidae 1Turtles Kachuga kachuga Hard shell tuttle Emydidae 2 2 nestsFish Seasonal Labeo rohita Rohu Cypinidae 5 R/YCatla catla Catla Cypinidae 2 R/YHeteropneustes fossilis Cat fish Saccobranchidae 12 R/YNote: *Globally Threatened, R/Y Round the year


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including amphibians, fish, certain turtles, gharial, mugger, dolphin and waterfowl consume the Benthos and fish. Gharial, mugger and dolphin are important tertiary players in the food chain but almost all of them are basically sympatric with each other in their feeding habits. Thus, they generally avoid each other for food and habitat or to say there is least competition among the various carnivores for food and space. Gharials hunt surface fishes, dolphins mostly depend on deep water fishes, otters may have habitat overlapping with dolphins, but muggers are totally different with respect to size and quantity of the prey. They generally feed on bigger prey. Birds to some extent certainly compete with muggers and gharials of lower age group for the small catch fish.

Pre- predatory and intra –predatory relationships are the least studied aspect in the NCS almost all the key stone species viz. gharial, gangetic dolphin and mugger are pisivorous species. Illegal fishing on commercial scales has reduce in the availability of chief prey in the NCS which may have a direct bearing on the reduced numbers of the above species especially that of gharials. Birds prey, some of the migratory birds, jackles, monitor lizards, carnivores and omnivore turtles prey upon eggs and hatchlings of gharial and mugger. This intra-predatory relationship controls the natural recruitment of gharial and muggers. Thus, it becomes very important to study pre-predator and intra-predatory relationships to maintain dynamic and viable populations of keystone species in the site.

Figure 2. Food pyramid diagram of National Chambal Sanctuary (NCS), India.

Population directly dependent upon wetland resources and cultural-indigenous practices of wetland resource utilization

As detailed elsewhere more than four lakes population is directly dependent on the river ecosystem. They invariably cultivate the land up to the brim, pump out the water for irrigation purposes. Agricultural practices up to the brim of the river to some extent certainly adversely affect the nesting behavior of gharials, muggers and turtles. Fishing is almost through the length of the sanctuary. Fishing on commercial scales is most prevalent in NCS.

There are many fake owners who auction the fishing permits every year to small traders. The fishing activity in recent times is gravely affected actual numbers of gharial and mugger population. Once caught in to the fishing nets these creatures get entangled and then beaten to death to relieve the fishing nets. Simultaneously fishing activity also reduces the food availability for tertiary components of the biological pyramid (keystone species). Sand mining is the major detrimental activity that is destructing the habitat in a highly dangerous way. Recent survey of NCS and the court commissioner's report has brought out some disturbing picture of habitat destruction and highly mortality of wild animals (Anon. 2003).

Existing conservation measures National Chambal Sanctuary is one of the rare protected

areas where good levels of conservation measures were successfully taken up and implemented. Gharial rehabilitation project was started in the year 1979 when all time low gharials were recorded (50 gharials as per report of science today report in 1979). Deori has been designated as Gharial Rehabilitation Centre (DGRC) where artificial hatching and rearing of gharials was carried out. In all 1287 gharials were released into the sanctuary. Initially there was no much pressure with respect to resource and utilization on to the Chambal Ecosystem. Then people were law obedient and had fear for administration. There was a spirit of team work that resulted in better conservation measures as reflected in above table. But, as a result of gradual political and muscle power getting into lucrative sand mining business over a period of 10-15 years, people have become more daring and destructive. Unabated illegal sand extraction in many stretches of the NCS resulted in severe habitat destruction and reduction in number of gharials. Even the migratory avifauna is being hunted mercilessly in the NCS. Around 37 animals were found dead during the survey of the year 2003. The casualties included 8 gharials, 2 muggers, 1 dolphin, 7 turtles and several birds. The high rate of mortality of wild animals caused by illegal fishing and mining is a matter of serious concern. Additional boon for NCS is simultaneous conservation of one of the rarest and highly endangered aquatic mammal i.e. fresh water river dolphin (Gangetic Dolphin) during implementation of gharial project. Results of the recent survey indicated that the number of gharials dwindled almost less than 50% in comparison to 1997 estimated population. Regular monitoring could have saved the NCS. NCS on the river Chambal is a refuge for the rare and endangered gharial (Gavialis gangeticus) and ganges river dolphin (Platanista gangetica). The Chambal river is holding the best population of dolphins among the southern tributaries of Ganges. The 400 km stretch of crystal clear water also supports marsh crocodiles, smooth coated otters, 7 species of turtles (Asperidetes gangeticus, Lissemys punctata, Chitra indica, Kachuga kachuga, K. dhongoka, Pangshura tentoria and Hardella thurgii) and 250 species of birds. The Chambal river also supports more than 40 species of fish species, which include Deccan mahseer Tor khudree and the giant fresh water ray Himantura chaophraya, which occur only in the Chambal river

Gharial, Otter,

Mugger, Dolphin,

Fish eating turtles Fish eating birds

Turtles, Fishes & Water fowl

Macrophytes

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(Taigor and Rao 2010). A good population of Indian Skimmers is the strongest birding attraction here. Black Bellied Terns, Red Crested and Ferruginous Poachards, Bar-Headed Goose, Sarus Crane, Great Thick-Knee, Indian Courser, Pallas's Fish Eagle, Pallid Harrier, Greater and Lesser Flamingos, Darters, and the resident Brown Hawk Owl, all add up to an impressive list of birds of Chambal. The habitat of aquatic animals in the Chambal river is characterized by expanses of open sand which is sparsely covered with the variety of herbs, the most common in the open sand being Tamarix dioca. Some Turtle species frequently dig nest adjacent to the T. dioca on some occasions soft shell turtles also dig nests near this vegetation. The T. dioca on the open sand help prevent the wind from eroding the sand and exposing nests. Aquatic and semi-aquatic vegetation are similar along the entire Chambal river. Herbivorous Turtles feed and take shelter on T. dioca, Potamogeton demersum, and Zennichelia spp. vegetation. During summer the aquatic vegetation dries up due to low water level, however, during wet season the vegetation is completely submerged in the flood waters and it is difficult to collect the plant material during this period. Major tree species are Prosopis spp., Acacia spp., Zizyphus marutiana etc. Turtle, Asperderetes gangeticus travel more than 500 m and lay eggs under the shade of Acacia spp.( Taigor and Rao, 2010).

The habitat of the fauna in NCS is mostly aquatic with terrestrial habitat within 1 km from the mid river bank. The micro habitats are: deep water pools, shallow riffle areas, sand peninsulas, muddy banks, sand banks (steep and sand banks), rocky banks, xerophytes vegetation on the banks etc. The habitat as the key to organizing knowledge about fauna and maintenance of appropriate habitat is the foundation of all wildlife management (Thomas 1979). Species richness can be affected by habitat loss, fragmentation and modification. Habitat studies provide crucial information about the ecological requirements of a species or community. Increasing habitat loss causes a significant increase in extinction risk among many species. The management criteria in the NCS are cessation of commercial fishing, anti-poaching measures, extending protection to habitat and rehabilitation of Gharial under 'grow and release programme' and monitoring of the population of fauna and research (Singh, 1985).

CONCLUSIONS

Observations of NCS were considerably altered and there are disturbances by the sand miners, poachers, fishermen and farmers. Considering the poor survival, it is recommended to provide greater protection by management practices. Effective co-operations between the Forest Department of Madhya Pradesh and bordering states are needed as sand mining and poaching becomes an interstate

problem. Thus, strategic location of this site in the migratory route of water birds enhances its importance as a significant water bird habitat. NCS Management Plan 2003 gives very good account of avifauna of the NCS. It over- emphasizes significant and important birds species available in the NCS which are of National and International importance. Crocodiles use sand banks for nesting and basking. Fauna in the NCS is very much influenced by various factors like habitat suitability and protection of their habitats. Their distribution is depending on availability of deep water pools. Another important factor on which distribution of animals depends is long stretches of long sand banks. Sloppy and steep sand bank with loose soil are essential for good habitats for nesting of crocodiles, turtles and birds. NCS will have negative impact mainly on the Gharial, Turtle breeding programmes and other avifauna.

ACKNOWLEDGEMENT

Author is thankful to Dr. M.S. Negi, Director, Tropical Forest Research Institute, Jabalpur for providing the necessary facilities. Author is highly indebted to Divisional Forest Officer, Forest Division, Morena, M.P. for providing the field facilities. Author is also grateful to Dr. R.K. Sharma, Range Officer, National Chambal Sanctuary, Deori (Morena),Madhya Pradesh, India for identifying the fauna.

REFERENCES

Ali S, Vijayan VS (1986) Keoladev National Park Ecology Study. Summer Report. 1980-1985. Bombay Nat. His. Soc. Bombay.

Anon (2003) National Chambal Sanctuary Management Plan. Forest Division, Morena, Madhya Pradesh, 35 pp.

Ganeshaiah KN, Chandrasekara K, Kumar ARV (1997) A new measure of biodiversity based on biological heterogeneity of the communities. Curr Sci73: 128-133.

Railsback SF, Stauffer HB, Harvey BC (2003) What can habitat preference modes tell us? Tests using a vitual trout population. Ecol Appl 13 :1580-1594.

Rao RJ (1988) Nesting ecology of the gharial in the National Chambal Sanctuary, WII, Mimeo.105.

Rao RJ (1990) Ecological relationships among freshwater turtles in the Natonal Chambal Sanctuary. Study Report WII, Mimeo, 1-212.

Singh LAK (1985) Gharial Population Trend in National Chambal Sanctuary with notes on radio-tracking. Study Report Dec. 1985. Crocodile Research Centre, Wildlife Institute of India, Hyderabad.

Singh LAK (1978) Ecological studies on the Indian Gharial Gavialis gangeticus (Gmelin) (Reptilia, Crocodilia) [Dissertation]. Utkal University, Bhubaneswar.

Taigor SR, Rao RJ ( 2010) Habitat features of aquatic animals in the National Chambal Sanctuary, Madhya Pradesh. Asian J. Exp. Biol. Sci. 1: 409-414.

Thomas JW (1979) Wildlife habitat in managed forests: The blue Mountain of Oregon. U.S.D.A. Forest Service Handbook 553, Washington, D.C.


Biodiversities and limiting factors of Lashgardar Protected Area (LPA), Hamadan Province, Iran

MAHDI REYAHI KHORAM1,♥, VAHID NORISHARIKABAD2 1Department of Environment, School of the Basic Knowledge, Islamic Azad University- Hamadan Branch, P.O.BOX: 65155-184, Hamadan, Iran. Tel:

+98811 8268595. Fax: +98811 4494170. ♥email: [email protected]

2Graduate School of the Environment and Energy, Islamic Azad University- science and Research Branch in Tehran, Tel: +98811 9131933595. Fax: +98811 4226162. email: [email protected]

Manuscript received: 30 July 2010. Revision accepted: 4 September 2010.

ABSTRACT

Reyahi-Khoram M, Norisharikabad V (2011) Biodiversities and limiting factors of Lashgardar Protected Area (LPA), Hamadan Province, Iran. Biodiversitas 12: 216-221. Lashgardar Protected Area (LPA) located in Hamadan Province in Iran, it is a mountainous and plain area and proximal to Malayer Township. In 1991, the region was known as a protected area for increasing wild animals' population. This research has been conducted during 2001 through 2009. Plant and animal species of the region were identified and statistics of the population of animal flagship species were gathered. In this research, valid academic resources were used for identification of animal and plant species. Geographic Information System (GIS) has been used to evaluate the land as main tool. The software used was Arc View (version 3.2a) scale was 1/50,000. Due to cold mountainous climate, the region is covered by a wide diversity of trees, shrubs, grasses and herbs. There were 18 species of mammals as well as 75 bird species in LPA. Most abundant mammalian population belongs to wild sheep (558 animals) and the second abundance was related to wild goat (515 animals). Also, the most abundant bird species belong to ortolans. Result of the present study showed that construction of connection roads in vicinity the region, establishment of factories inside and around the region, military garrison, unauthorized grazing, unlawful hunting, and Ahangaran mine and rail road have all exposed put LPA to serious threat and danger.

Key words: biodiversity, environment, Lashgardar, protected area, wildlife.

INTRODUCTION

At the onset of life on the earth, land was covered with various plant and animal species and consequently full of natural resources, which had always been exposed to transformations due to geological evolutions and climatic changes. Such changes happened very quickly sometimes, but occurred much slowly at most times. Although as regards quality and quantity, these changes could never be compared to the changes Made by Human Hands. The human power is regarded as a very powerful factor in changing the living conditions of plants and animals, which has led to destruction of habitats and deterioration of genetic resources. Hasty measures and interferences of human in the habitats have led to reduction of species, extinction of a remarkable diversity of species, and loss of biodiversity. Therefore, those concerned with environment issues have considered strategies on international level so as to protect the biodiversity. A protected area is an area, which has been determined specifically for protection and maintenance of its biodiversity, natural and cultural resources, and is protected and controlled through legal measures or common traditional methods. In fact, protected areas are the manifests of creation and their protection is the fundamental basis for activities of environmentalists (Najmizadeh and Yavari 2006).

Protection of biodiversity and genetic Diversity could reliably support the goals of development. Today's, the process of destruction of habitats has outrivaled restoration and reconstruction. Extinction of species in all growth ecosystems has had a soaring increase and once the scientists do not investigate and solve this crisis, within a short time it would threaten the life of many plant and animal species.

Today, biodiversity is prone to threat even in protected areas. Destruction of habitats and their turning into islands has put long-term protection of many protected habitats in dilemma. Wildlife habitats are areas in which undomesticated species of plant or animal could find their food, water and shelter needs and other required necessities for survival. It is estimated that 5000 species of mammals, 10000 species of birds, 8000 species of reptiles, 5500 species of amphibious and 27000 species of fishes or aquatics exist throughout the world (Nunes-Paulo et al. 2003). A recent study in Iran has shown that Iran with about 1.65 million square kilometer surface area is a large country and after Turkey is the richest country in plant diversity in the Middle East. The rich flora and fauna and unique landscapes of this land and its old civilization attracted many biologists and orientalists (Jafari and Akhani 2008).The climatic diversity of Iran has resulted in the growth of 7576 plant species, the occurrence of 517 bird species, 208 reptile species, 170 fish species, 164

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mammal species and 22 amphibians (Reyahi-Khoram et al., 2010). The general acceptance of the concept of protected areas in Iran and the necessity to allocate areas to them which was materialized by the foundation of three national parks and 15 protected areas in 1967 is considered a turning point in the history of the environmental protection in Iran. Continuous increase in the number, area and diversity of the protected areas over the last 40 year documented protection history of Iran indicated public awareness and will to protect biological resources and reserves. Designation of 160 protected areas of the total area of 11824599 hectares until 2006 covering 7.17 percent of the entire country area indicates an annual increase rate of 4.2 areas and 311174 hectares (Darvishsefat 2006). LPA being Located in Hamadan Province, it is a mountainous and plain area and proximity to population centers as Malayer Township have facilitated educational, research and tourist activities in the region. Malayer is one of the cities of Hamadan province in west of Iran.

With expansion of environmental Knowledge and valuable activities of Non governmental Organization (NGO), the necessity of protection of plant and animal habitats and the areas under management of Department of Environment (DoE) with the aim of developing ecotourism, biodiversity, and research and educational affairs becomes more clear every day so that everyone understands its importance. In the ecosystems of arid and semi-arid regions, as Iran, the issue of protection becomes more important because the ecosystems are fragile.


This research has been conducted during 2001 through 2009. Documentary and observation methods have been used to access to information. This means that identifying biodiversities and limitations of the LPA was made during the research years through extensive field inspections and direct field observations. Plant and animal species of the region were identified and statistics of the population of animal flagship species were gathered. In this research, valid academic resources were used for identification of animal and plant species (Ziaie 1996; Mansoori 2001).

To identify and define ecologic resources of the region, digital maps were used and on this basis the topology situations as well as ground cover of studied area have been accomplished. In addition, Geographic Information System (GIS), Remote sensing tools and technology were used in determining any changes in this study area and evaluate the land. The software used was Arc View (version 3.2a) with the Universal Transverse Mercator (UTM) projection and scale was 1/50,000.


General status of the region LPA with 24,000 hectares surface area is situated

between 34º,09',00'' and 34º,20',00'' northern latitudes and

between 48º,51',30'' and 49º,02',00''eastern longitudes, on northern highlands of Malayer Township in Hamadan Province. "Koh Sardeh" Mountain with a height of 2858 meters from sea level is in northern part of the region. The rocks of this mountain are the main habitat of wild goats(Capra aegagrus) Also dune-bedded parts of this region are known to be the main habitat of wild sheep. Ahangaran Mountain with altitude of 2758 m is in the southeastern part of the region (Figure 1). This is a high rocky mountain with several valleys, appropriate ground cover and sufficient expansion, which has created suitable conditions for survival of flagship species. Based on the initial investigations made by the experts of DoE in October 1984, this region was officially declared as a prohibited hunting area for five years. For the second time in 1989, this region was officially announced as a prohibited hunting area for another three years. Finally, in 1991, the region was known as a protected area for increasing wild animals' population. In order to manage and control of LPA, two units ranger's station (Police Station) located in the western area and north area of the region are fully controlling and supervising the region by several facility and with full equipment.

Because of the type of land application, plain regions of the studied area are suitable mainly for agricultural activities and pasture management. The rocky areas with sleep slopes, cliffs, caves, deep valleys are suitable for reproduction of different species of wild animals and passing the winter season. High mountains cause snow precipitation, which in turn is very effective to recharge the underground water table. In reciprocal interaction, soil and ground cover help survival and stability of ecosystem.

The studied area has average water resources. This means that the water need of different animal and plant species are supplied through permanent and seasonal water springs. This region has 11 permanent springs of which; only five springs have been sanitized and improved. There is not any permanent river in LPA. The only seasonal river of this region is Jozan-Aznaveleh, which is rooted in Gomasab Babolghani Mountains and joins Haramabad River after passing through the region. Because it is a seasonal river, no aquatic lives in it and no aquatic bird can make nest there. Regarding the situation of springs, the wild sheep(Ovis orientalis) have easy access to water. Also, some springs such as Ozon Dareh flow from the heights to near the plain regions. LPA is a mountainous area, minimum altitude of 1750 meters in plain regions and maximum altitude of 2858 meters in Koh Sardeh Mountains.

According to statistics of meteorological stations, maximum ambient temperature in summer is 36.8ºc in July, while the minimum is 6.5ºc below zero in January. The amount of annual precipitation is different from 250 millimeters in plain regions to 320 millimeters in the heights. Most of the precipitations occurred in the form of snow in cold months of the year. Average relative humidity of the area is 28% in the hottest month (July) and 70% in the most humid month (March).


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Figure 1. General status of Lashgardar Protected Area (A) in Hamadan Province (B).

Wind direction is south-north in this region. Also the

ground level of these regions is covered with rock land, which is in turn influenced by wind blow, i.e. due to wind blow the soil surface layer undergoes corrosion and will find no chance for improvement. In the winter due to high wind speed, wild animals are mostly seen in the lowest part of the region. But in summer, the animals choose the southern rocky part of the region which is a leeward part as their daylong sleeping and grazing.

Unfortunately no watershed management project has been implemented in the region. Therefore a small amount of water from precipitations infiltrate to land, and land is quite dry in the heights. As a result of this, wild animals of Koh Sardeh Region, which are mainly wild goats, suffer from severe shortage of water in the summer.

There are 16 villages around the region. All villages are located in the border area of the region. The main business of these villagers is related to farming, gardening and animal husbandry. Whereas the villages' population has increased in recent years and the villages' economy is based on farming, gardening and animal husbandry and whereas there are a few free zones for animal grazing around the region, LPA suffer from animal grazing pressure.

Ahangaran lead and iron mine is in the eastern side of Ahangaran Mountains inside LPA. This mine was

exploited in 1960 for extraction of lead. Lead extraction from the depth of ground, tunnel excavation operations and soil withdraw created insecurity in the region. Therefore if a better method is used for extraction, its business is coordinated with the issue of protection. There is a garrison in the northeast part of the region. This place has been transferred to the army by the city's endowment department without coordination with DoE. Ozamen spring in the north of garrison is the main drinking pond for wild animals, which can hardly have access to it due to insecurity.

Regarding implementation of national and regional development programs in recent years, the need for establishment and expansion of connecting roads, railroads, electricity and gas supply lines have increased. These communication roads are mainly concentrated in the surrounding border area of the region.

Plant coverage of the region LPA has different plants so that most plant reserves of

Hamadan Province could be seen in this area. Based on the recent study that was accomplished in LPA, it was reported that, 43 families, 184 genera and 266 plant species are existed in LPA, almost 28 species of which are endemic of Iran (Safikhani et al. 2003). The most important medicinal plant species of LPA are: Gundelia tournefortii L.,

B A

Iran, Islamic Republic

Lashgardar Protected Area

Hamadan Province


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Carthamus tinctorius L., Rheum acuminatum, Ziziphora capitata L., Glycyrrhiza glabra, Plantago major L., Mentha logifolia (L). Hadson and Malva sylvestris. Due to cold mountainous climate, the region is covered by a wide diversity of trees, shrubs, grasses and herbs. But there is no forest area, shrub species are sporadically seen in the heights of the region and the most important shrub species of LPA are: Crataegus meyeri A. Pojark, Berberis integerrima Bunge and Amygdalus lycioides Spach. The most important tree species of LPA are ficus carica, Pistacia atlantica Desf and Rhus coriaria. The most important of herb and grass species of LPA are: Acantholimon olivieri (Jaub. & Spach) Boiss, Phlomis olivieri Benth, Achillea wilhelmsii C. Koch., Cicer oxyodon Boiss. & Hohen, Atraphaxis spinosa L., Zataria multiflora, Peganum harmala L, Echinops pungens Trautv, Fritillaria imperialis, Rheum ribes and Hypericum perforatum L.

Wildlife of the region There are 16 species of mammals from 11 families and

4 orders as well as 75 bird species from 23 families and 6 orders in LPA. The most mammal population belongs to wild sheep(Ovis orientalis) (558 animals) and the second abundance is related to wild goat (Capra aegagrus) (515 animals). Also, the most bird family belongs to Turdidae.

Mammals Due to the form of hoof and inability in escaping from

carnivores, wild goat (Capra aegagrus) is not interested in living in plain regions. It chooses its living place in mountainous and rocky places, and high lands with rocky partitions. The breeding season takes place in December. The lambs, usually two, are born in late May or June. This animal is territorial and protects its mating place. Among other characteristics of wild goat is that it does not migrate but lives as a native animal in the region. This behavior, beside the situation of ecological island of the area, i.e. its complete surrounding by human societies and expansion of agricultural, industrial and urban installations, has led to genetic equalization and jeopardizing this specie in the long term.

Wild sheep such as Armenian sheep (Ovis orientalis gmelini) and Esfahan sheep (Ovis orientalis isphahanica) too exist in western areas of the country. In LPA, the differences observed in the morphology of existing population indicate presence of hybrid species in the region; a white spot is seen in the waist of this specie, and these wild sheep are called "Allakamar", which by words means white-waist. Females are smaller than males and have short slightly curved horns. Due to natural behavioral characteristics and migration to Markazi province from the east of the region on one side, and migration to Nashr prohibited hunting area in Hamadan province and finally Ghazvin province, although this specie is subject to numerous hazards related to migration route.

On the other side, regarding the diversity of mammals, carnivores such as wolf (Canis lupus), Common fox (Vulpes vulpes), golden jackal (Canis aureus) and Striped Hyena (Hyaena hyaena) could be seen in the region. Daily and seasonal migrations of mammals play an important role

in their settlement in the region and they exist almost everywhere in the region. Other mammals with sufficient population as Afghan Pika (Ochotona rufescens), Wild Boar (Sus Scrofa), Indian crested porcupine (Hystrix indica), Cape hare (Lepus capensis) and Yellow Ground Squirrel (Spermophilus fulvus) specie live in the region. Figure 2 and 3 summarize the distribution of mammal orders and species in the studied area.

Due to regular and efficient protection so far, the process of growth of two important species of the region, including wild goat and wild sheep indicates favorite growth of population of these species in recent years so that the total population of wild goat reached from 117 animals in 1999 to 515 animals in 2009. Wild sheep population reached from 127 animals in 1999 to 558 animals at the end of 2009 year. The population growths related to wild sheep and wiled goat are shown in Figure 4. Optimum increase of population has led to issuance of hunting permit of these species to respond to the demands of the hunters in the region so that in 2003, 22 special permits were issued (15 for wild sheep and 7 for wild goat) and in 2009, 15 permits including 10 permits for wild sheep and 5 permits for wild goat were issued. Certainly substantial habitat characteristics as the most important factors have played their role in improvement of biotic conditions.

Birds With varied plain, foothill and mountainous ecosystems

and also an intact pasture and shrub coverage, beside fruit orchards close to the region, LPA has managed to successfully play its role as a suitable habitat for different family of birds. The most bird population is related to Turdidae family and the highest percent of abundance is related to Passeriformes order (69%) including Alaudidae, Motacillidae, Laniidae, Turdidae, Sylviidae, Sittidae, Emberizidae, Fringillidae, Ploceidae, Sturnidae and Corvidae families. After this, Falconiformes order with 11% presence and finally Caprimulgiformes order with 1% has minimum abundance of LPA. Figure 5 summarizes the distribution of bird orders and families in the studied area.

Figure 2. Classification of mammal orders in LPA of the year 2009

Artiodactyla65%

Carnivora11%

Lagomorpha3%

Rodentia21%


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Discussion The present results showed that LPA, as a

natural environment it has a diversity and expansion of different plant and animal species and in fact, it is necessary to protect this region as an animal and plant habitat. In addition, LPA has many appropriate industrial and economic development capabilities, but as a natural environment it has a diversity of plant and animal species. Field observations and studies showed that construction of connection roads in vicinity the region, establishment of factories inside and around the region, military garrison, unauthorized grazing, unlawful hunting, and Ahangaran mine and rail road have all put LPA in serious threat and danger. Therefore it is extremely necessary that LPA management intensify its protective and security measures with full alertness for survival of wildlife of the region. A few management studies that have been carried out have focused on the improvement of management and environmental education activities in protected areas (Xu J. et al. 2006); (Geneletti and Iris 2008). Meliadis et al. (2009) reported that current technologies can be used for modeling environmental parameters which improve our knowledge of the attributes, characteristics, situation, trends, and changes of natural ecosystems in the protected area.

It is also quite necessary to take appropriate measures and make useful interference in the said LPA in order to improve and stabilize the existing conditions. It is obvious that the suggested interfering measures are provisional, which are aimed at stabilizing and improving the existing conditions; otherwise man has no right to interfere in natural characteristics of the region.

The obtained results showed that in this region water resources are mainly permanent and seasonal springs and no water shortage is seen in most times of the year. But watershed management studies and implementation of watershed projects will result in controlling water and soil corrosion and maintenance. Due to the existence of rocky areas with sleep slopes, cliffs in the rocks, deep valleys and dune-bedded areas with different valleys, this region has provided suitable conditions for reproduction and passing winter season of different species of wildlife.

LPA has a diversity of mountainous plants and because of cold weather, it has a rich coverage of shrubs and grasses in the heights and pasture plants in dune-bedded hills. Therefore the region's animal has no special critical problem regarding forage and food. Also with regard to construction of two units ranger's House in the said region and by employing experienced rangers, the region's security coefficient increases too, although some shortages could also be seen in these areas.

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CONCLUSION

These results, and previous studies, indicated that expansion of road lines, highways and railroads around the region created problems related to migration routes of the wild animals of the region by hindering the genetic transfer from one generation to the other. The author sure that this factor can prevents the genetic diversity which in turn is responsible for species diversity, because the wild animals in free zones and in LPA have little chance of migration due to permanent traffic of vehicles. In the meantime wild animals need in-migrations and out-migrations with free habitants in order to pass winter season, reproduction and other habitat needs. It has been observed that species like cape hare (Lepus capensis), golden jackal (Canis aureus) and Striped Hyena (Hyaena hyaena) clash with vehicles when they are migrating and die. Permanent traffic of vehicles in these roads has its influences on wildlife restriction due to creating insecurity.

RECOMMENDATIONS

Because of migrations the wildlife, it is recommended that the migration route related to wildlife be organized to studying and designing roads and it is necessary to attend the construct of underpass for wildlife migration. Since management of the LPA is very important, it is highly recommended that consultant of LPA plan should accelerate to complete and approve the guideline for the preparation of management plans for LPA. From a practical perspective, authorities may consider controlling drought and preparing the region's watershed management plan and implementing necessary mechanical and biomechanical installations as well as management strategies in a timely manner. It is recommended that the authorities consider providing sufficient credit to identify, determine the parcel national lands and people-owned lands of studied area and purchase un-national lands and obtain legal document for all lands in the entire region. Since carrying capacity studying is very important related to environmental management, it is suggested that the authorities consider identify the carrying capability of LPA and determining the number of wild animals and their reproduction in the near future.

ACKNOWLEDGMENTS

This research was supported by Hamadan Provincial Directorate of Environmental Protection, to which the authors’ thanks are due. The authors also thank Mr. Mohammad pour, the head of Hamadan Provincial Directorate of Environmental Protection, for their collaboration in this study. Also special thanks to Adel Arabi and Mahdi Safikhani, the experts of Environmental Protection in hamadan province and other experts for their participation.

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Forest land use by the community in Sorong Natural Tourism Park at Sorong City, West Papua Province

YOHANES YOSEPH RAHAWARIN Faculty of Forestry, the State University of Papua, Jl. Gunung Salju, Amban-Manokwari 98314, West Papua, Indonesia, Tel & Fax.: +62-986-211364,

email: [email protected]

Manuscript received: 2 June 2010. Revision accepted: 14 August 2010.

ABSTRACT

Rahawarin Y (2011) Forest land use by the community in Sorong Natural Tourism Park at Sorong City, West Papua Province. Biodiversitas 12: 222-227. The aim of the research was to: (i) identify the type and extent of forest land use alteration at Sorong Natural Tourism Park (or SNTP), (ii) investigate society activities that cause forest land use alteration, and (iii) make the zoning level of environmental damage (iv) investigate the causative factors of forest land use alteration at SNTP. The method used was survey with field observation and semi-structural interview techniques. The primary data of biophysical aspects consist of type and extents of land usage by society; while data of socio-cultural aspects consist of level of community dependency upon land and the existing of local institution and management of SNTP. Secondary data that had been collected consist of study results documentation and report of SNTP management aspects. Data were analyzed by using (i) qualitative descriptive analysis of society socio-cultural and management aspects, (ii) spatial analysis of biophysical aspects, and (iii) environmental analysis of biophysical, socio-cultural and management aspects. Evaluation of environmental analysis was used to arrange directive and environmental management strategy at SNTP. Result of research indicated that since its establishment in 1981 to 2009, SNTP forest land utilizing for settlements, forest product extraction and shifting cultivation activity by society had been cause of land use alteration occurred which was incompatible with area function about 11,53%. Changing in the land use caused by society activities in land utilizes such settlements, forest product extraction and shifting cultivation. Level of environmental degradation in the catchments area of damage SNTP level indicates that 8.01% of total of land area was in slightly damaged, 2.36% was moderately damaged and 1.16% is in heavily damaged. Inadequate support on socio-cultural aspects of society at SNTP and the lack of founding and supervising upon SNTP management was pointed as causative factors on environmental damage. Based on level of environmental damage, community based forest management system will be able to be implemented as environmental management strategy at SNTP.

Key words: forest land use, environmental degradation, Sorong Natural Tourism Park.

INTRODUCTION

Forest is a multifunctional natural resources in support of human life, not only as a place for the conservation of biodiversity and maintenance of ecosystem functions, but also to produce goods and services for the community. The forest area in Papua has the potential of natural resources with a rich diversity that is high enough, by requiring the protection, conservation and sustainable use to maintain its diversity. Conservation, also function as a protected area, area also has other functions such as life-support systems and as a means of research and development of science, education, nature tourism and support for aquaculture activities. Sorong Natural Tourism Park (SNTP) or “Taman Wisata Alam (TWA) Sorong” is a tourism park located in the province of West Papua. It has a high biodiversity and is based on the Decree of the Minister of Agriculture No. 397/Kpts/Um/5/1981 date may 1981 07 a surface of 945.9 ha (MoA 1981; BKSDA West Papua 2007). This region serves as a nature which can be exploited for tourism and recreation natural conservation area.

The existence of the conservation area at this time usually undergoes a variety of incredible pressure. There is

no conservation area which is free from illegal activity, either in form of illegal logging, poaching, the invasion of the area for growing, settlements, exploration and exploitation of minerals, land use conflicts or other uses. Moga (2005) suggested that the cause of the destruction of the area of conservation was because of the weakness of the social aspects of the surrounding community. Nitibaskara (2005) said that there was institutional limitations of Government which was responsible for the management of conservation, as the weakness of the growth of the population, especially in the communities around the edge of the forest area reduction policy areas.

Sorong Natural Tourism Park is adjacent to the location of the residential areas. It is resulted in the interruption of the broadening of the forests. This area has becomed the stone angle society needed to meet the needs of everyday life. Some of the internal effects among others are settlement in the region, the forest for activities not related to the conservation and agriculture, gardens and fields, the use of wood and other forest products, mainly for land use firewood, illegal to local needs, logging hunting and trapping in the region. External effects with predominantly happen among others are wildlife and move the fields on

RAHAWARIN – Forest land use in Sorong Natural Tourism Park

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the form, the use of the area of conservation for other purposes such as mining and others, as well as the construction of roads in the area of conservation overlay.

Negative impact of such utilization is reduction recharge area in SNTP region. It can lead to surface runoff and erosion causes floods, landslides or during the rainy season. It is caused of because the loss of trees with its wide crown serving as water retention. A way that can be done to overcome the negative impact is that by increasing the flow of groundwater of infiltration. Several impacts of logging activity is a threat to environmental damage of SNTP. This research aims to analyze the form and the extensive use SNTP , to analyze forest land utilization by people around, the effect damage emerged and to analyze the effect factors of the cause of land use change.


Data collection The method used in the research was survey with field

observation and semi-structural interview techniques. Biophysical aspects of primary data consist of the shape and the use of soil and vegetation cover area. Socio-cultural of society aspects, including the degree of dependence of the population of the land and the Community institutions and the SNTP management data. Secondary data are achieved from documents/reports the results of research related to aspects of management of SNTP. Secondary data is done through listing documents or research reports.

Land use change There is forest land utilization done by the people

around in the forest land. In order to know the location, the form, and the land use change, the tracking through GPS is implemented. The data obtained are spatially processed in a way to calculate the area of overlapping polygons using an ArcView GIS using version 3.3 of the program (FoGGMU 2009)

Catchment areas damage Processing of data for the analysis of damage to areas

of recharge used spatial analysis with scoring method (Kastaman et al. 2007). Natural environmental components affected the infiltration of outstanding potential, type of soil, and precipitation, whereas the land use affect the real infiltration land use. Score method with a system of classes based on Permenhut No. P.32/MENHUT-II/2009 (MoF 2009).

Socio-cultural aspects of society Aspects of weighting system and the parameters used in

the assessment of the socio-cultural aspects of society. The general formula used to calculate a value for each parameter of the aspects socio-cultural are: the indicator value = frequency x score x weight parameters. In addition, aspects of socio-cultural support for each parameter value is calculated based on the percentage weight of each parameter in the lowest and better qualifications.

Data analysis Parameters aspects management of SNTP observed

included the integrity of the boundaries of the area, if any bad supervision and guidance to the public. The descriptive data processing based on interviews and comments field, and information as well as secondary data. Data analysis was performed by: (i) qualitative descriptive analysis for the social aspects of public culture and parameters management SNTP, (ii) the spatial analysis of the aspects of Biophysics (land-use change), and (iii) an environmental assessment for the biofisk, aspects social and cultural manajamen region, which later became the basis in the formulation of the direction and strategies for environmental management of SNTP.


Land use change Land use activities

SNTP laid down in the Decree of the Minister of agriculture No.397/Kpst/UM/I/1981 area of 945.90 hectares per day in October 2009 Note research occurred during the use of the soil that is incompatible with the region in SNTP functions. SNTP land-use change began around the year 1998, starting with the public for a variety of needs, land use activities both for settlements, forest product extraction and shifting cultivation.

Type and size of land use The results of measurement and analysis of spatial

forms of land are known that from the total SNTP land of 945.9 Ha, the converted areas for others used about 109.06 hectares (11.53%). The form and area land use SNTP are presented in Table 1, and spatially depicted in thematic land use such as shown in Figure 1.

Table 1. Type and land use area of SNTP

Location and type of land use Area (ha)

Percentage (%)

Inform-ation

Garden and field Klasaman village 5.30 0.56 2 plot Klablim village 19.29 2.04 11 plot

Sub-total 24.59 2.60 Settlement Klasaman village 0.38 0.04 1 plot Klablim village 7.85 0.83 2 plot

Sub-total 8.23 0.87 Shrub Klasaman village 1.89 0.20 2 plot Klablim village 73.87 7.81 1 plot

Sub-total 75.76 8.01 Open land Klasaman village 0.47 0.05 1 plot

Lowland forest Klasaman and Klablim village 836.81 88.47

Total 945.9 100.00


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Figure 1. The map land use in Sorong Natural Tourism Park (SNTP)

The results of Table 1 and Figure 1 shows the largest land conversion is a shrub (8.01%), followed by plantations/crops (2.60%), residential (0.87%) and open field (0.05%), while the rest continue forming lowland forests (88.47%). Due to the availability of the road and the entrance to the forests of the community to facilitate development of housing, gardening fields area land use change/and forest harvesting. Basuni et al. (2009) said that human activity is usually inside and outside the area of conservation, particularly in unregulated land use and become a threat to the sustainability of the area of conservation. Whenthe threat is permanent, without end (eternal external threat) thenland conservation areas and their products will remain the limited resources for a growing population.

Catchment areas damage Potential infiltration

Potential penetration values obtained from the type of soil and factors slope factor rain infiltration in SNTP. Precipitation infiltration coefficient will be multiplied by the amount of precipitation divided into 100 days with rain. On the basis of climatic data (BMG Sorong 2009) showed that the rainfall over the last 10 years (1999-2008) was 2887.40 mm, the number of rainy days as many as 218 days, precipitation infiltration 6295 mm, including classification of very large (> 5500 mm). Forest land in SNTP is divided into two kinds of Brown podzolic and

alluvial soils. Brown podsol ability penetration is fairly large, and alluvial soils are classified as small. SNTP conditions slope with flat areas (0-8%) and slope (8-15%).

Spatial analysis results showed that 90.06% of SNTP able to absorb the water with great skill, while the rest (9.94%) is of average size water infiltration. Hamzah (1975) in Tokede (1989) states the ability to store water forest soils depends largely on the percentage of silt and clay. The higher the percentage, the more water is stored, it is not excessive humidity that can lead to poor soil aeration. Commonly known that the growth of trees in clay soils are better than in clay or sandy soil.

Actual infiltration Land use, vegetation cover mainly affects the

infiltration through three forms, namely: the root and the pores enlarge permeabiitas soil, vegetation cover to hold run-off and vegetation cover reduces the amount of percolation of water through transpiration. Canopy trees falling rain erosivity power to change is by changing the speed and grain size of rain drops. Factors that contribute to high canopy cover, canopy thickness, density, so the garbage, grass and herbs as ground cover. Given the role of vegetation cover and or use of land in SNTP region, the value of the actual infiltration rate of the area, then based on qualitative Permenhut No P.32/MENHUT-II/2009 (MoF 2009) presented in Table 2.


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Table 2. Classification value of actual infiltration of SNTP Type of land use Scale closure Value of actual infiltration Low land forest 76-100% large Shrub 51-75% small large Garden and field 25-60% moderate Settlement 0.5-25% rather small Open land < 0.5% small Source: Modified from Barbour et al. (1987); Indriyanto (2006); MDNR (2007); MoF (2009).

Table 2 explains that this area of land is in various

forms of land use conversion above have resulted changes in the level of cover. SNTP forest serving act to protect the interests of biology nature conservation area. The

ecological function of natural processes that took place became interrupted due to changes in the abundance of cover, such as pressure and threats the diversity of species and changes in patterns of succession of forests and the diversity of species and the community in a landscape patterns.

Forest areas opening activity SNTP society to be used as a bird capture zones acted by vegetation cover. The development of settlement by municipality Klasaman activities, Srahwata and Kolam Susu coatings intend to reduce the abundance and spread community activities that make rotation of crops through the opening of the gardens or the fields in this area.. Thus, abundance decline due to development solution from SNTP, land use change coverage collection of forest products and gardening

activities or agriculture is a threat of damage to the environment if not properly managed will threaten the existence of functional areas.

The level of damage of recharge area

The results of spatial analysis with overlay and scoring method between the potential of thematic infiltration and actual infiltration thematic. Based on the analysis, it is true that the thematic level of damage catchment areas are in accordance with Permenhut No. P.32/MENHUT-II/2009, as it is shown in Figure 2. Based on Figure 2 it is known that the change in the land use caused by society activities in land utilizes such settlements, forest product extraction and shifting cultivation. Level of environmental degradation in the catchments area of damage SNTP level indicates that 75.77 ha (8.01%) is in slightly damaged, 2.36 ha (2.36%) is in moderate damaged and 10.97 ha (1.16%) is in heavily damaged. The damage of the recharge area is caused by land use change with little abudance of land cover and also spread of rarely so that it emerges bigger surface stream. Changing in the use and ground vegetation cover hydrological is very influential in quantities. In this case, it is the amount of infiltration so that regions with a level of abundance and cover will be much better then recharge water. It is good and natural. On the other hand, the more scarce the land over and damage, the higher the damage level of recharge area (Bruce 1966 in Nurlita 2008).

Figure 2. The map of damage level of recharge area in SNTP


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Table 3. Indicator value support social and cultural aspects of society against environmental managemnet SNTP

Socio-cultural aspects Village SNTP Klasaman Klablim Level of dependence of population on land Land area moderate (6.50) less (4.68) moderate (5.59) Land status very strong (5.98) strong (4.55) very strong (5.27) Livelihood diversification moderate (3.55) moderate (3.75) moderate (3.65) Distribution and allocation of work time less (1.71) moderate (1.98) moderate (1.85) Special customs and traditions strong (2.38) strong (2.45) strong (2.42)

Total value (1) strong (20.12) moderate (17.41) moderate (18.77) Community institutions Institutional activity less (3.15) less (2.42) less (2.78) Forms and functions of institutions less (2.59) moderate (3.50) moderate (3.05)

Total value (2) less (5.74) less (5.92) less (5.83) Total value of socio-cultural aspects (1) + (2) moderate (25.86) moderate (23.33) moderate (24.59)

Changing in forest cover to be housing, the open ground, bush and the dry land crop will reduce the ability to store the ground water supplies. This is in accordance with the proposal of Rauf (2009), the ability of the land to absorb the water varies depend on the characteristic of the soil, soil management, and in particular of the soil coverage itself. Forest land can absorb more water than land-use. According to Fahmuddin et al. (2004), when the use of forest land is converted into other use, soil, plants and the hydrological cycle in it are also influenced. This is because the impact caused by the physical, biological and chemical changes as well as the life on earth that is above them. Also be aware of the system of management of the land used for other functions, especially biodiversity is lost because of the convertion forest land.

The factors of environmental damage of SNTP Socio-cultural aspects of society

The results of socio-cultural support the management of the SNTP area can be seen in Table 3. Table 3 shows that the level of dependency of the population on the land which remains weak contribution (18.77) against the management of SNTP. This fact can be seen in the contribution of less support far-reaching general land, livelihoods diversification and the distribution allocation of work time. This situation illustrates the possibility of strong enough environmental damages of SNTP to support the contribution of the aspects of the dependence of the population in the land for the management of the area. The parameters of the socio-cultural aspects of society that describes support for tradition is strong and the support of land use is very strong. According to Ekawati et al (2008) the state of the farm that is carved out by the owner, there is a tendency to be managed in a sustainable manner. Conversely, if it is not managed by the owners of the land, there is a tendency of the land managed without taking into account aspects of conservation, because the user is more result oriented at the time.

The society custom is that taking benefit from the forest land fertility and potential environmental of SNTP relatively wide for their life. Purba (2005) says that agricultural systems that move periodically (rotated) are very adaptable to the environment and forests show proven

wisdom environment suitable for the preservation of the biodiversity of tropical forests. Thus, the degree of dependence of the population in an area that is strong and powerful reflects the status of land and traditions contributing to the community in supporting the efforts to preserve the region against the threat of environmental damage.

The lack of institutional aspects of the society to support the efforts of environmental management SNTP, is cause the form and function of local institution which is not fully involved in the management area. Apart from that, the absence of local instituion activity provides support for the conservation and management of SNTP. The activities of management are inactive and the institutions are likely waiting for instruction from government institutions. According to Purba (2005), the plan and the implementation of the social environment management that are carried out by local government will not always guarantee community of people to always be able to get the best benefits in the environmental management to improve social welfare. The principle of the social environment management must give greater priority to the participation of the community and the community as a whole. Tokede et al. (2008) explained that forest management based on community of people is characterized by specific typology of forestry society that the final goal is the empowerment and welfare society.

The aspects of the SNTP management The results showed that optimal development activities

have not been done so and are still limited to the public in general as students, university student of Sorong. Illumination to people in both towns has not done well. This is clearly seen from existance of different point of view how about the community should participate in the management of the SNTP. The main limitation is the shortage of human resources and operational support. Based on field observations and interviews with people and officials, it is known that many landmarks are broken or gone, which are intentionally pulled out or broken in the landmark of SNTP. The landmarks which are built since the beginning are not taken care well.The nursing such as painting and giving new number are not done yet. Based on


227

the description of the aspects of area management, it is known that the incompleteness of the boundary region since it is broken, gone and the not optimum directing activity to society caused by the work control of SNTP.

Environmental management strategy of SNTP In general, management policies are divided into three

parts namely technical policy (water and soil conservation), socio-cultural address and the policy guidelines. Technical policy is in the form of activities and the implementation of reforestation and agroforestry systems. Socio-cultural policies referred to forest management systems based on community. Policy guidelines aimed at changing the paradigm of the management of single stakeholder to many stakeholders. SNTP strategies of management is done through the following activities: (i) the stabilisation of the region, (ii) the formulation of the area, (iii) construction of infrastructure and facilities for recreation and tourism nature, (iv) the potential area management, (v) protection of the area, (vi) the research and education, (vii) the management of nature tourism, and (viii) development of cross-sectoral integration and coordination.

CONCLUSIONS AND RECOMMENDATIONS

Since established in 1981 until 2009, the activity of taking benefit from SNTP by community around (urbanization, forest product extraction and gardening or shifting cultivation activities) has led to a change of land use for 11.53%. The conversion of SNTP forest land to be housing and open field has increased of damage recharge area for 10.97 ha (1.16%) to be badly damage; 22.36 ha (2.36%) was in damage condition in the form of plantation land; 75.77 ha (8.01%) was in rather damage in the form of bush. The lack the support of social and cultural society and the ineffective supervision and monitoring of management activities are factors of the cause of environmental damage in SNTP. Based on the level of damage and the factors cause of environmental damage, SNTP environment management strategies can be implemented through forest management system based on community that includes a number of activities, namely: (i) the stabilization of the region, (ii) preparing a management plan that could accommodate the participation of communities and other stakeholders, (iii) construction of infrastructure and facilities for recreation and tourism nature, (iv) the potential area management, (v) the protection and security of the area, (vi), research and educational activities, (vii) the management of nature tourism (viii) development of cross-sectoral integration and coordination.

The need of approach changing paradigm in the management of SNTP from single stakeholder to many stakeholders with basic management change, namely from government based management to multi stakeholders based management (collaborative management). Improvement

and prevention toward the existence of threat to SNTP environmental damage can be done with involving surrounding people in reforestation and the implementation of agroforestry through forest management systems based on community.

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Authors Index

Abbas B 112 Abbot LK 145 Abdulhadi R 187 Abedi R 182 Adhikerana AS 46 Ahmad F 118 Amin M 69 Ardaka IM 15 Ariyanti EE 124 Bintoro MH 112 Bratawinata AA 204 Budiharta S 151 Bustam BM 9, 129 Dewiyanti I 139 Djuuna IAF 145 Ehara H 112 Fitri L 129 Gibson B 200 Iskandar E 55 Junaedi DI 75 Jusuf M 187 Karwa A 97 Khoram MR 216 Kuntorini EM 102 Kusmana C 187 Kyes RC 55 Lestari Y 65 Marwoto B 176 Meshram PK 211 Mirmanto E 82 Mudiana D 124 Mutaqien Z 75 Nelly N 93 Norisharikabad V 216 Nugroho LH 102 Nurmeiliasari 200 Pamoengkas P 34 Pangastuti A 65 Perwitasari-Farajallah D 55 Poerba YS 118 Pourbabaei H 182 Putranto HD 200 Rahawarin YY 222

Rahayu S 187 Rai MK 97, 157 Renwarin Y 112 Ruchaemi A 204 Rusli R 93 Saharjo BH 40 Shahabuddin 29 Sidik AS 204 Siregar HM 15 Siregar IZ 5, 107 Siregar M 15 Siregar UJ 107 Soetrisno E 200 Subahar TSS 24 Sudarsono 112 Sudo S 40 Sugardjito J 46 Sugiyarto 89 Suharsono 187 Suhartono 59 Suhartono MT 65 Sumardi I 167 Sunaryanto R 176 Surahman M 112 Sutarno 1, 89 Suwanto A 65 Suwarno 19 Suyatna I 204 Taurusman AA 133 Tsuruta H 40 Van Niel K 145 Widodo 89 Widoretno S 89 Wilujeng S 194 Wulandari M 167 Yaherwandi 93 Yonemura S 40 Yuliana A 24 Yunanto T 5 Yusmarika F 93 Zueni A 200 Zulfahmi 107

Subject Index

Aceh 5, 87, 130, 132, 139, 140,

144 Agaricus 97, 98, 101 alang-alang 39-44 AM Fungi 145-149, 165 anatomical character 167, 168, 170, 172 antibiotic 59, 63, 64, 68, 98, 129-

132, 176-178, 180, 181 antimicrobial activity 176-178, 181 Austrostipa 9, 10, 12-14 bacterial community 65-68, 132 Bali Botanic Garden 15-18 banana cultivar 118, 122, 123, 167-175 Begonia “Tuti Siregar” 15-18 biodiversity 4, 5, 24, 25, 28-36, 39,

40, 45, 46, 52, 54, 80-81,87, 89, 92,, 97, 100, 111, 117, 128, 141, 149, 151, 152, 154-157, 162, 165-167, 176, 182-183, 185, 186, 192, 212, 215-217, 221, 222, 226

biodiversity protection area 151, 152, 154, 155 biomass burning 40, 41, 44, 45 biotechnological strategies 157, 164 Bosscha Observatory 24, 25, 28 Brassicaceae 93-96, 111 bulb 102-106, butterfly diversity 24, 25, 27, 28, canonical correspondence analysis 204, 205 Central Kalimantan 35, 82, 87, 88, 154, 156 chloroplast DNA 107, 109, 111-114, 117,

193 chloroplast microsatellites 107, 108, 111, 117 coastal water 133, 134, 138, 210 community 23-25, 28-30, 32-34, 42,

65-68, 76, 80, 82, 85-87, cooking bananas 118, 119, 121 deforestation 29, 33, 37, 45-47, 49, 52,

53, 54, 92, 151, 156, 182, 198, 199

demersal fish 204-210 development 3, 16, 19, 20, 22-25, 27-

28, 34-39, 44, 46, 49, 52, 53, 55, 65-70, 72-74, 82, 87, 89,90, 101-107, 111, 117, 124-128, 133, 145, 146, 150, 154, 157-158, 160-166, 169, 170, 175, 180-182, 188, 192, 194, 196, 197, 199, 204, 210, 216, 218, 220, 222, 224-227

dipterocarp species 34-37, 111, 152, 154, 155 Dipterocarpaceae 35, 36, 46, 82, 83, 107,

111, 112, 117, 151, 153-155, 198

diversity 1, 4, 5, 8, 24, 25, 27-34, 37, 40, 45, 52-57, 65-70,

73, 75, 81, 83-85, 87, 89-98, 100, 101, 107, 109, 110-112, 114-118, 122, 123, 133, 137, 138, 145, 148-151, 153-157, 163, 166, 168, 182-187, 190, 192-194, 198, 204-206, 210-214, 216, 217, 219-222, 225

DNA banks 157, 163-166 domination 25, 79, 194, 198 dung beetles 29-32 electrophoresis 2, 6, 8, 59, 60, 63-65,

108, 119, 177 Eleutherine americana 102, 106 environment 3, 8, 19, 23-25, 27, 28,

34, 35, 37, 40-42, 44, 45, 52, 54, 67, 75, 82-85, 91-93, 98, 100, 101, 103, 105, 107, 115, 118, 124, 129, 133, 136-138-142, 144-149, 155, 165-167,178, 185-187, 189, 191, 192, 194, 196-199, 204-210, 216, 217, 220-223, 225-227

environmental degradation 222, 225, estrous cycle 200-203 eutrophication 133-136 evenness 65-67, 151, 153-155, 182-

186 fauna 23, 28, 32-34, 91, 133,

135, 138, 150, 210-213, 215

feeding guild 133-138 floristic composition 82, 85, 87, 88, 151, 153-

156 flow of genetic intervention 69 flower and fruit development 124-128 flowering 8, 16, 18, 25-27, 87, 91,

92, 111, 124, 127, 128, 154, 192, 194, 196, 197, 199

forest conversion 29, 31, 33, 151, forest land use 47, 54, 222 GAM 145-149 Ganoderma 97, 100 Gede Pangrango National Park 155, 156, 187, 192 genetic diversity 1, 5, 8, 56, 57, 70, 89,

100, 107, 110, 112, 115-118, 122, 123, 157, 163, 187, 192, 216, 221

genetic variation 1, 3, 4, 8, 57, 58, 73, 74, 92, 107, 109, 111, 116, 117, 120, 123, 189, 192

GH gene 1, 8 GLM 145-149 GOT 5-8 grassland rhizosphere 129, 130

growth 1-4, 12, 19, 20, 23, 34-39, 46, 60, 61, 65, 68, 70, 72, 74, 75, 87, 88, 98, 103, 104, 106, 111, 117, 129-132, 136, 145, 149, 150, 154, 156-158, 160-166, 168, 17, 175, 178, 180, 186, 188, 191, 192, 197-199, 216, 219, 220, 222, 224

Guilan 182-186 habitat fragmentation 24, 46, 52, 54, 80, 81 habitat selection 29, 32 haplotype 112-112, 114-117 High Conservation Value Forest (HCVF)

151, 156

host plant 20, 22, 24-28, 93, 187 Hoya multiflora 187-193 imagery 46, 47 immature stages 19-21, 23, 93, Indonesia 1-5, 15, 18, 24, 28, 29,

30, 33-37, 40,41, 45-47, 52-56, 58, 65, 69, 73, 74, 79-82, 87-88, 92, 96, 107, 108, 111-113, 116, 117, 123, 129, 133,134, 137-140, 144, 151-152, 156, 158, 159, 167, 168, 170, 175, 176, 187, 188, 192, 194, 200-204, 206, 210,

Indonesian local cattle 2, 3 inheritance and linkage 5, 8 isolation 2, 60, 61, 66, 98, 100,

108, 112, 113, 129-132, 155, 176-178, 181

isozyme 5-8 Jakarta Bay 133-138 land use 24, 29, 30-33, 38, 40, 44,

46-54, 98, 145-150, 199, 221-227

Landsat 46, 47, 51 large plasmids 59-64 Lashgardar 216-218 leaf 10, 13-18, 22, 39, 93, 97,

102-105, 108, 113, 117, 119, 139-142, 144, 150, 159, 161-163, 166-168, 170-175, 186, 188, 189, 191-193, 195, 199

leaves litter 139, 144 Lepidoptera 19, 22, 23, 28, 93-96, 213 Litopenaeus vannamei 65, 67, 68 local cattle 2, 3, 69, 70, 73 long-tailed macaques 55-58 Macaca fascicularis 55-58 macrozoobenthos 133-138 Mahakam delta 204-208, 210 main stands 89-92 marine Actinomycetes 176-181 marker assisted selection 1, 3, 4, 162 mass loss 139-142 medicinal 81, 97, 98, 100, 151, 157-

160, 162-166, 187, 218 medicinal plants 97, 157, 158, 160, 162,

164-166, micro morphological 9-14 microbes 67, 129-132, 142, 161,

164, 165 micropropagation 157-159, 164-166 microsatellite 55-58, 107-111, 117, 164 minimum inhibitory concentration 176, 178-180, 179 molecular 1, 3, 4, 9, 42, 58, 60-65,

67, 106, 108, 109, 111-114, 116-118, 122, 123, 132, 162-164, 167, 168

morphological diversity 187 morphology 12-14, 16, 60, 68, 91, 97,

128, 130, 167, 168, 170, 171, 173-176, 178, 181, 189, 192, 219,

Mount Patuha 75, 80, 81 mtDNA 1, 2, 73, Musa acuminata 118, 119, 121, 123, 167,

168, 171-173, 175 Musa balbisiana 118, 119, 121, 167, 168,

171-173 mushrooms 97, 98, 100, 101 mycorrhization 157, 159, 160, 162, 164-

166 naphtoquinone 102, 103, 105, 106 national chambal sanctuary 211, 212, 214, 215 natural enemies 19-23 new cultivar 15, 16, 18 nutrients 87, 98, 135, 139, 144,

160, 185 Papilio polytes 19-23, 26, 27, parasitoid 19-23, 93-96 PCR-RFLP 1, 2, 3 peat grass 40-44 peat soil 40-44 peat-swamp 82-87 PFGE 59, 60, 63, 64 phenotypic variation 6, 69, 71 Pinus merkusii 5-8, 89 plant ecology 33, 39, 75, 92, 111, 117,

150, 227 plantain 33, 118, 122, 123, 175 Pleurotus 97, 100 ploidy level 167-170, 172-174 population 3, 4, 8, 19-23, 27,32, 34,

41, 42, 46, 53-59, 63, 68, 69, 73, 74, 78-81, 90, 93-95, 107-118, 122, 123, 129, 132, 140, 149, 150, 151, 155, 160, 163, 178, 182, 187-189, 191-194, 196, 197, 199-201, 205, 211, 213-220, 222, 223, 224, 226

population dynamic 19, 21-23, 57, 68 production forest 34, 35, 75, 151, 156 production landscape 151, 156, 182, RAPD analysis 111, 118 RE (restriction enzyme) 2-3, 59-64, 66, 67, remnant forest 75 Rhizophora stylosa 139-144 richness 24, 29-33, 36, 66, 67, 81,

83-86, 89-93, 100, 101, 151, 153, 154, 156, 182, 184-186, 204-206, 212, 213, 215

Rural Heritage Museum 182-186 sago palm 112-117 sambar deer 200-203

screening 58, 118, 129, 132, 161, 165, 166, 176, 178, 181

seasonal effect 200, 201, 203 seasons 19-23, 96, 98, 100, 194,

197, 199, 201, 202, 205, 212

Sebangau 91, 96, 97, 101, 128, 132-134, 136-138, 144, 155, 186, 192, 196, 197, 205, 206, 210, 215, 222-227

selective cutting and line planting 34-36 selective logging 30, 33, 34, 53, 82 sexual behavior 200-203 Shorea acuminata 107-110 social groups 55-57 soil quality 34-36, 38, 39 Sorong Natural Tourism Park 222, 224, 227 Sowang 194, 196-199 standard walk 24, 25 stipoid grasses 9, 12, 14 Syzygium pycnanthum 124-128 taxonomic diversity 89, 90

trace gas 40, 42, 44, 45 transformation 31, 157, 162-166 trawl 204, 205, 209, 210 tree communities 54, 75, 77, 79, 80 T-RFLP 65-68 uropathogenic E. coli 59, 63 variations 1, 6, 54, 55, 58, 73, 83,

117, 125, 133, 135, 169, 187-189, 192

vegetation 23, 28-30, 32-37, 39-43, 45-47, 75-77, 80-92, 98, 139-141, 144, 146, 149, 156, 182, 183-186, 196, 199, 214, 215, 223-225, 227

Wanagama 89-92 water depth 137, 204-206, 208, 209,

212 wildlife 28, 53, 81, 151, 156, 203,

215,216, 219-222 Xanthostemon novaguineense 194, 195, 197-199

List of Peer Reviewers

Abd Fattah N. Abd Rabou Department of Biology, Faculty of Science, Islamic University of Gaza, Palestine Agung Kurniawan Bali Botanic Garden, Indonesian Institute of Science (LIPI), Tabanan, Bali, Indonesia Ahmad Dwi Setyawan Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University,

Surakarta, Central Java, Indonesia Akira Itoh Laboratory of Plant Ecology, Graduate School of Science, Osaka City University, Japan Alan J. Lymbery Division of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Australia Ali Saad Mohamed College of Veterinary Medicine, Sudan University of Science and Technology, Khartoum, North-

Sudan Alfonds Andrew Maramis Biology Department, Faculty of Mathematics and Natural Sciences, State University of Manado,

Tondano, North of Sulawesi, Indonesia Am Azbas Taurusman Department of Utilization of Fisheries Resources, Faculty of Fisheries and Marine Sciences, Bogor

Agricultural University, Bogor, West Java, Indonesia Artini Pangastuti Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University,

Surakarta, Central Java, Indonesia Bambang Hero Saharjo Forest Fire Laboratory, Department of Silviculture, Faculty of Forestry, Bogor Agricultural

University, Bogor, West Java, Indonesia Bambang Sulistiyarto Christian University of Palangkaraya, Palangkaraya, Central Kalimantan, Indonesia Betty Mauliya Bustam Department of Biology, Faculty of Mathematics and Natural Sciences, Syiah Kuala University,

Banda Aceh, Nangroe Aceh Darussalam, Indonesia Bradley Bergstrom Department of Biology, Valdosta State University, Valdosta, GA, USA Charis Amarantini Faculty of Biology, Duta Wacana Christian University, Yogyakarta, Indonesia Cristina Cruz Department of Zoology and Anthropology, Faculty of Sciences, Universidade do Porto, Portugal Cynthia Fowler Society of Ethnobiology, Wofford College, Spartanburg, SC, USA Daiane H. Nunes Department of Agronomy, State University of Londrina, Londrina, Brazil Danielle Kreb RASI – Conservation Foundation, Samarinda, East Kalimantan, Indonesia Deden Mudiana Purwodadi Botanical Garden, Indonesian Institute of Sciences, Pasuruan, East Java, Indonesia Dewi Ayu Lestari Purwodadi Botanical Garden, Indonesian Institute of Sciences, Pasuruan, East Java, Indonesia Dirk Holscher Division of Tropical Silviculture and Forest Ecology, Faculty of Forest Sciences and Forest

Ecology, Georg-August University, Göttingen, Germany Djoko Purnomo Faculty of Agriculture, Sebelas Maret University, Surakarta, Indonesia Dwi Hastuti Stabilization Office of Forest Area XI, Ministry of Forestry, Yogyakarta, Indonesia Dwi Murti Puspitaningtyas Center for Plant Conservation, Bogor Botanical Garden, Indonesian Institute of Sciences, Bogor,

West Java, Indonesia Edi Rudi Department of Biology, Faculty of Mathematics and Natural Sciences, Syiah Kuala University,

Banda Aceh, Nangroe Aceh Darussalam, Indonesia Eizi Suzuki Earth and Environmental Sciences,Graduate School of Science and Engineering, Kagoshima

University, Japan Esti Endah Ariyanti Purwodadi Botanical Garden, Indonesian Institute of Sciences, Pasuruan, East Java, Indonesia Fitmawati Department of Biology, Faculty of Mathematics and Natural Sciences, State University of Riau,

Pekanbaru, Riau, Indonesia Freddy Pattiselanno Animal Production Laboratory, Animal Science, Fishery & Marine Sciences, State University of

Papua, Manokwari, West Papua, Indonesia Gono Semiadi Zoology Division, Research Center for Biology, Indonesian Institute of Sciences, Cibinong-Bogor,

West Java, Indonesia Guofan Shao Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, USA Hapry Fred Nico Lapian Faculty of Animal Science, Sam Ratulangi University, Manado, North Sulawesi, Indonesia Haryono Zoology Division, Research Center for Biology, Indonesian Institute of Sciences, Cibinong-Bogor,

West Java, Indonesia Hwan Su Yoon Bigelow Laboratory for Ocean Sciences, McKown Point Road, West Boothbay Harbor, ME, USA Irnanda Aiko Fifi Juuna Department of Soil Sciences, Faculty of Agriculture and Agriculture Technology, State University

of Papua, Manokwari, West Papua, Indonesia.

Iskandar Z. Siregar Department of Silviculture, Faculty of Forestry, Bogor Agricultural University, Bogor, West Java, Indonesia

Issirep Sumardi Faculty of Biology, Gadjah Mada University, Yogyakarta, Indonesia Jamsari Plant Breeding Section, Faculty of Agriculture, Andalas University, Padang, West Sumatra,

Indonesia Joko Ridho Witono Center for Plant Conservation, Bogor Botanical Garden, Indonesian Institute of Sciences, Bogor,

West Java, Indonesia Kanika Sharma Microbial Research Laboratory, Department of Botany, University College of Science, M.L.

Sukhadia University, Udaipur, India Kristamtini Assessment Institute for Agricultural Technology Yogyakarta, Ministry of Agriculture,

Yogyakarta, Indonesia Lily Surayya Eka Putri Department of Biology, Faculty of Science and Technology, State Islamic University Syarif

Hidayatullah Jakarta, Indonesia Livia Wanntorp Department of Phanerogamic Botany, Swedish Museum of Natural History, Stockholm, Sweden Luitgard Schwendenmann School of Environment, University of Auckland, New Zealand Made Sri Prana Botany Division, Research Center for Biology, Indonesian Institute of Sciences, Cibinong-Bogor,

West Java, Indonesia Magdy H. Abd El-Twab Department of Botany and Microbiology, Faculty of Science, Minia University, El-Minia City,

Egypt Magdy Ibrahim El-Bana Department of Biology, College of Teacher, King Saud University, Riyadh, Saudi Arabia Mahendra Kumar Rai Department of Biotechnology, SGB Amravati University, Maharashtra, India Manuela Winkler

Institute of Botany, Department of Integrative Biology, University of Natural Resources and Applied Life Sciences, Vienna, Austria

María de los Ángeles La Torre Cuadros

Department of Forest Management, Faculty of Forestry Sciences, National Agrarian University, La Molina, Lima, Peru

Maria Teresa Manfredi

Department of Animal Pathology, Hygiene and Veterinary Public Health, Universita Studi degli di Milano, Italy

Medi Hendra Biology Department, Faculty of Mathematics and Natural Sciences, Mulawarman University, Samarinda, East Kalimantan, Indonesia

Mera Wulandari Faculty of Biology, Gadjah Mada University, Yogyakarta, Indonesia Mochamad Arief Soendjoto Faculty of Forestry, Lambung Mangkurat University, Banjarbaru, South Kalimantan, Indonesia, Nina Dwi Yulia Purwodadi Botanic Garden, Indonesian Institute of Sciences, Pasuruan, East Java, Indonesia Nur Fadli Department of Biology, Faculty of Mathematics and Natural Sciences, Syiah Kuala University,

Banda Aceh, Nangroe Aceh Darussalam, Indonesia Onrizal Department of Forestry, Faculty of Agriculture, North Sumatra University, Medan, North Sumatra,

Indonesia Peter C. Boyce School of Biological Sciences, Universiti Sains Malaysia, Pulau Pinang, Malaysia Phillip T.O. Raburu Fisheries Department, Moi University, Eldoret, Kenya R. Susanti Department of Biology, Faculty of Mathematics and Natural Sciences, Semarang State University,

Semarang, Central Java, Indonesia. Rofiq Sunaryanto Center of Biotechnology, Agency for the Assessment and Application Technology, South

Tangerang, Banten, Indonesia Serafinah Indriyani Biology Department, Faculty of Mathematics and Natural Sciences, Brawijaya University, Malang,

East Java, Indonesia. Shahabuddin Faculty of Agriculture, Tadulako University, Tondo, Palu, Central Sulawesi, Indonesia Shao-yun He Department of Horticulture, South China Agricultural University, Guangzhou, P.R. China Simone M. Scheffer-Basso Universidade de Passo Fundo, Bairro São José, Brazil Siti Sofiah Purwodadi Botanic Garden, Indonesian Institute of Sciences, Pasuruan, East Java, Indonesia Skyler J. Hackley University of California, Santa Cruz, CA, USA and Ecosystems Center, Marine Biological

Laboratory, Woods Hole, MA, USA Sri Wilujeng

Biology Program, Department of Mathematics and Basic Science Education, Faculty of Education, Cendrawasih University, Jayapura, Papua, Indonesia

Sugardjito Zoology Division, Research Center for Biology, Indonesian Institute of Sciences, Cibinong-Bogor, West Java, Indonesia

Sugiyarto Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University, Surakarta, Central Java, Indonesia

Suhadi Department of Biology, Faculty of Mathematics and Natural Sciences, State University of Malang, Malang, East Java, Indonesia

Suhartono Department of Biology, Faculty of Mathematics and Natural Sciences, Syiah Kuala University, Banda Aceh, Nangroe Aceh Darussalam, Indonesia

Sundaram Seshadri Shri AMM Murugappa Chettiar Research Centre, Taramani, Chennai, India Supyani Faculty of Agriculture, Sebelas Maret University, Surakarta, Indonesia Sutarno Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University,

Surakarta, Central Java, Indonesia Tati Suryati S. Subahar School of Life Sciences & Technology, Bandung Institute of Technology, Bandung, West Java,

Indonesia Thomas C. Wanger Environment Institute, School of Earth and Environmental Sciences, University of Adelaide,

Australia Titut Yulistyarini Purwodadi Botanic Garden, Indonesian Institute of Sciences, Pasuruan, East Java, Indonesia Tiziano Bo Department of Life and Environmental Science, University of Piemonte Orientale, Alessandria,

Italy Udhi Eko Hernawan Research Center for Oceanography, Indonesian Institute of Sciences, Tual, Southeast Maluku,

Indonesia Utaminingsih Faculty of Biology, Gadjah Mada University, Yogyakarta, Indonesia Wilhelm Barthlott Nees-Institute for Biodiversity of Plants, Bonn, Germany Wiryono Faculty of Agriculture, Bengkulu University, Bengkulu, Indonesia Yaya Ihya Ulumuddin Research Center for Oceanography, Indonesian Institute of Sciences, North Jakarta, Indonesia Yekki Yasmin Department of Biology, Faculty of Mathematics and Natural Sciences, Syiah Kuala University,

Banda Aceh, Nangroe Aceh Darussalam, Indonesia Yohan Rusiyantoro Department of Animal Science, Faculty of Agriculture, University of Tadulako, Tondo Palu,

Indonesia Yohanes Y. Rahawarin Faculty of Forestry, State University of Papua, Manokwari, West Papua, Indonesia Yuyu Suryasari Poerba Botany Division, Research Center for Biology, Indonesian Institute of Sciences, Cibinong-Bogor,

West Java, Indonesia Zaenal Mutaqien Cibodas Botanical Garden, Indonesian Institute of Sciences, Cianjur, West Java, Indonesia Zhu Hua Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, P.R. China Zumaidar Department of Biology, Faculty of Mathematics and Natural Sciences, Syiah Kuala University,

Banda Aceh, Nangroe Aceh Darussalam, Indonesia

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GUIDANCE FOR AUTHORS

BIODIVERSITAS, the Journal of Biological Diversity publishes scientific articles, i.e. original research and review in all biodiversity aspects of plants, animals and microbes at the level of gene, species, and ecosystem. Scientific feedback (short communication) is only received for manuscript, which criticize published article before. Manuscripts will be reviewed by managing editor and invited peer review according to their disciplines. The only articles written in English (U.S. English) are accepted for publication. This journal periodically publishes in January, April, July, and October. In order to support reduction of global warming as a consequence of transportation vehicles emission and forest degradation for paper manufacturing, management of the journal prefer receiving manuscripts via e-mail rather than in hard copy. Manuscript and its communications can only be addressed to the managing editor; better to “CC” to one of the communicating editor for accelerating evaluation. A letter of statement expressing that the author (s) is responsible for the original content of manuscript, the result of author(s)’s research and never been published must be attached.

Manuscript is typed at one side of white paper of A4 (210x297 mm2) size, in a single column, double space, 12-point Times New Roman font, with 2 cm distance step aside in all side. Smaller letter size and space can be applied in presenting table. Word processing program or additional software can be used, however, it must be PC compatible and Microsoft Word based. Names of sub-species until phylum should be written in italic, except for italic sentence. Scientific name (genera, species, author), and cultivar or strain should be mentioned completely at the first time mentioning it, especially for taxonomic manuscripts. Name of genera can be shortened after first mentioning, except generating confusion. Name of author can be eliminated after first mentioning. For example, Rhizopus oryzae L. UICC 524, hereinafter can be written as R. oryzae UICC 524. Using trivial name should be avoided, otherwise generating confusion. Mentioning of scientific name completely can be repeated at Materials and Methods. Biochemical and chemical nomenclature should follow the order of IUPAC-IUB, while its translation to Indonesian-English refers to Glossarium Istilah Asing-Indonesia (2006). For DNA sequence, it is better used Courier New font.

Symbols of standard chemical and abbreviation of chemistry name can be applied for common and clear used, for example, completely written butilic hydroxytoluene to be BHT hereinafter. Metric measurement use IS denomination, usage other system should follow the value of equivalent with the denomination of IS first mentioning. Abbreviation set of, like g, mg, mL, etc. do not follow by dot. Minus index (m-2, L-1, h-1) suggested to be used, except in things like “per-plant” or “per-plot”. Equation of mathematics does not always can be written down in one column with text, for that case can be written separately. Number one to ten are expressed with words, except if it relates to measurement, while values above them written in number, except in early sentence. Fraction should be expressed in decimal. In text, it should be used “%” rather than “gratuity”. Avoid expressing idea with complicated sentence and verbiage, and used efficient and effective sentence. Manuscript of original research should be written in no more than 25 pages (including tables and picture), each page contain 700-800 word, or proportional with article in this publication number. Invited review articles will be accommodated.

Title of article should be written in compact, clear, and informative sentence preferably not more than 20 words. Name of author(s) should be completely written. Running title is about five words. Name and institution address should be also completely written with street name and number (location), zip code, telephone number, facsimile number, and e-mail address. Manuscript written by a group, author for correspondence along with address is required. First page of the manuscript is used for writing above information.

Abstract should not be more than 200 words, written in English. Keywords is about five words, covering scientific and local name (if any), research theme, and special methods which used. Introduction is about 400-600 words, covering background and aims of the research. Materials and Methods should emphasize on the procedures and data analysis. Results and Discussion should be written as a series of connecting sentences, however, for manuscript with long discussion should be divided into sub titles. Thorough discussion represents the causal effect mainly explains for why and how the results of the research were taken place, and do not only re-express the mentioned results in the form of sentences. Concluding sentence should preferably be given at the end of the discussion. Acknowledgments are expressed in a brief.

Figures and Tables of maximum of three pages should be clearly presented. Title of a picture is written down below the picture, while title of a table is written in the above the table. Colored picture and photo can be accepted if information in manuscript can lose without those images. Photos

and pictures are preferably presented in a digital file. JPEG format should be sent in the final (accepted) article. Author could consign any picture or photo for front cover, although it does not print in the manuscript. There is no appendix, all data or data analysis are incorporated into Results and Discussions. For broad data, it can be displayed in website as Supplement.

Citation in manuscript is written in “name and year” system; and is arranged from oldest to newest and from A to Z. The sentence sourced from many authors, should be structured based on the year of recently. In citing an article written by two authors, both of them should be mentioned, however, for three and more authors only the family (last) name of the first author is mentioned followed by et al., for example: Saharjo and Nurhayati (2006) or (Boonkerd 2003a, b, c; Sugiyarto 2004; El-Bana and Nijs 2005; Balagadde et al. 2008; Webb et al. 2008). Extent citation as shown with word “cit” should be avoided, and suggested to refer an original reference.

APA style in double space is used in the journal reference as follow: Journal: Carranza S, Arnold EN (2006) Systematics, biogeography and evolution of

Hemidactylus geckos (Reptilia: Gekkonidae) elucidated using mitochondrial DNA sequences. Mol Phylogenet Evol 38: 531-545.

Saharjo BH, Nurhayati AD (2006) Domination and composition structure change at hemic peat natural regeneration following burning; a case study in Pelalawan, Riau Province. Biodiversitas 7: 154-158.

Book: Rai MK, Carpinella C (2006) Naturally occurring bioactive compounds.

Elsevier, Amsterdam. Chapter in book: Webb CO, Cannon CH, Davies SJ (2008) Ecological organization,

biogeography, and the phylogenetic structure of rainforest tree communities. In: Carson W, Schnitzer S (eds) Tropical forest community ecology. Wiley-Blackwell, New York.

Abstract: Assaeed AM (2007) Seed production and dispersal of Rhazya stricta. 50th

annual symposium of the International Association for Vegetation Science, Swansea, UK, 23-27 July 2007.

Proceeding: Alikodra HS (2000) Biodiversity for development of local autonomous

government. In: Setyawan AD, Sutarno (eds) Toward mount Lawu national park; proceeding of national seminary and workshop on biodiversity conservation to protect and save germplasm in Java island. Sebelas Maret University, Surakarta, 17-20 July 2000. [Indonesian]

Thesis, Dissertation: Sugiyarto (2004) Soil macro-invertebrates diversity and inter-cropping plants

productivity in agroforestry system based on sengon. [Dissertation]. Brawijaya University, Malang. [Indonesian]

Information from internet: Balagadde FK, Song H, Ozaki J, Collins CH, Barnet M, Arnold FH, Quake

SR, You L (2008) A synthetic Escherichia coli predator-prey ecosystem. Mol Syst Biol 4: 187. www.molecularsystemsbiology.com Publication manuscript “in press” can be cited and mentioned in

reference (bibliography); “personal communications” can be cited, but cannot be mentioned in reference. Research which not be published or “submitted” cannot be cited.

Some annotation. Manuscript typed without sign link (-) (except repeated word in Indonesian). Usage of letter “l” (el) to “1” (one) or “O” (oh) to “0” (null) should be avoided. Symbols of α, β, χ, etc. included through facility of insert, non altering letter type. No space between words and punctuation mark.

Progress of manuscript. Notification of manuscript whether it is accepted or refused will be notified in about three months since the manuscript received. Manuscript is refused if the content does not in line with the journal mission, low quality, inappropriate format, complicated language style, dishonesty of research authenticity, or no answer of correspondence in a certain period. Author or first authors at a group manuscript will get one original copy of journal containing manuscript submitted not more than a month after publication. Offprint or reprint is only available with special request.

NOTE: Author(s) agree to transfer copy right of published paper to BIODIVERSITAS, Journal of Biological Diversity. Authors shall no longer be allowed to publish manuscript completely without publisher permission. Authors or others allowed multiplying article in this journal as long as not for commercial purposes. For the new invention, authors suggested to manage its patent before publishing in this journal.

NOTIFICATION: All communications are strongly recommended to be undertaken through email.

SPECIES DIVERSTY

Anatomy and morphology character of five Indonesian banana cultivars (Musa spp.) based on their ploidy level ISSIREP SUMARDI, MERA WULANDARI

167-175

ECOSYSTEM DIVERSTY

Marine Actinomycetes screening of Banten West Coast and their antibiotics purification ROFIQ SUNARYANTO, BAMBANG MARWOTO

176-181

Plant diversity in natural forest of Guilan Rural Heritage Museum in Iran ROYA ABEDI, HASSAN POURBABAEI

182-186

Morphological variation of Hoya multiflora Blume at different habitat type of Bodogol Research Station of Gunung Gede Pangrango Natonal Park, Indonesia SRI RAHAYU, MUHAMMAD JUSUF, SUHARSONO, CECEP KUSMANA, ROCHADI ABDULHADI

187-193

The effects of forest burning and logging toward regeneration ability of Sowang (Xanthostemon novaguineense Valet.) in Cycloop Mountain, Jayapura, Papua SRI WILUJENG

194-199

Recognition of seasonal effect on captive Sumatran Sambar deer reproductive cyclicity and sexual behaviors HERI DWI PUTRANTO, EDI SOETRISNO, NURMEILIASARI, AHMAD ZUENI, BERRY GIBSON

200-203

Demersal fishes and their distribution in estuarine waters of Mahakam Delta, East Kalimantan IWAN SUYATNA, ACHMAD ARIFFIEN BRATAWINATA, ACHMAD SYAFEI SIDIK, AFIF RUCHAEMI

204-210

Diversity of some fauna in National Chambal Sanctuary in Madhya Pradesh, India PREMANAND KALKRISHANA MESHRAM

211-215

Biodiversities and limiting factors of Lashgardar Protected Area (LPA), Hamadan Province, Iran MAHDI REYAHI KHORAM, VAHID NORISHARIKABAD

216-221

Forest land use by the community in Sorong Natural Tourism Park at Sorong City, West Papua Province YOHANES YOSEPH RAHAWARIN

222-227

Front cover: Cervus unicolor

(PHOTO: ABU ABDURRAHMAN)

Published four times in one year PRINTED IN INDONESIA

ISSN: 1412-033X (printed edition) ISSN: 2085-4722 (electronic)

ISSN: 2085-4722 (electronic) ISSN: 1412-033X (printed)

1412-033X (printed edition) ISSN: 2085-4722 (electronic)

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Transcript of 1412-033X (printed edition) ISSN: 2085-4722 (electronic)