Biodiversitas vol. 14, no. 1, April 2013 by Biodiversitas Unsjournals

ISSN: 1412-033X E-ISSN: 2085-4722

Journal of Biological Diversity Volume

14 – Number

1 – April

2013

ISSN/E-ISSN:

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

EDITORIAL BOARD (COMMUNICATING EDITORS):

Abdel Fattah N.A. Rabou (Palestine), Alan J. Lymbery (Australia), Bambang H. Saharjo (Indonesia), Daiane H. Nunes (Brazil), Edi Rudi (Indonesia), Guofan Shao (USA), Hassan Pourbabaei (Iran), Hwan Su Yoon (USA), I Made Sudiana (Indonesia), Joko R. Witono (Indonesia), Katsuhiko Kondo (Japan), Livia Wanntorp (Sweden), Mahendra K. Rai (India), María La Torre Cuadros (Peru), Mochamad A. Soendjoto (Indonesia), Shahabuddin (Indonesia), Sugiyarto (Indonesia)

EDITOR-IN-CHIEF: Sutarno

EDITORIAL MEMBERS:

English Editors: Suranto, Wiryono (wiryonogood@yahoo.com); Technical Editor & Banking: Solichatun (solichatun_s@yahoo.com) Distribution & Marketing: Rita Rakhmawati (oktia@yahoo.com); Webmaster: Ari Pitoyo (aripitoyo@yahoo.com)

MANAGING EDITORS:

Ahmad Dwi Setyawan (unsjournals@gmail.com)

PUBLISHER:

The Society for Indonesian Biodiversity

CO-PUBLISHER:

Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University, Surakarta

ADDRESS:

Jl. Ir. Sutami 36A Surakarta 57126. Tel. +62-271-7994097, Tel. & Fax.: +62-271-663375, Email: unsjournals@yahoo.com

BANKING:

Solichatun, BNI KC Sebelas Maret, Acc. No. 0033691646

ONLINE:

biodiversitas.mipa.uns.ac.id

EXPERTISE AND CORRESPONDING EMAIL OF THE COMMUNICATING EDITORS:

GENETIC DIVERSITY: Alan J. Lymbery (a.lymbery@murdoch.edu.au), Hwan Su Yoon (hsyoon@bigelow.org), Mahendra K. Rai (pmkrai@hotmail.com). SPECIES DIVERSITY: Joko R. Witono (jrwitono@yahoo.com), Katsuhiko Kondo (k3kondo@nodai.ac.jp), Livia Wanntorp (livia.wanntorp@nrm.se). ECOSYSTEM DIVERSITY: Abdel Fattah N.A. Rabou (arabou@iugaza.edu), Bambang H. Saharjo (bhsaharjo@gmail.com), Daiane H. Nunes (nunesdaiane@gmail.com), Edi Rudi (edirudi@yahoo.com), Guofan Shao (shao@purdue.edu), Hassan Pourbabaei (hassan_pourbabaei@yahoo.com), I Made Sudiana (sudianai@yahoo.com), Mochamad A. Soendjoto (masoendjoto@gmail.com), Shahabuddin (shahabsaleh@gmail.com), Sugiyarto (sugiyarto_ys@yahoo.com). ETHNOBIOLOGY: María La Torre Cuadros (angeleslatorre@lamolina.edu.pe).

Society for Indonesia Biodiversity

Sebelas Maret University Surakarta

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 1-9

ISSN: 1412-033X E-ISSN: 2085-4722 DOI: 10.13057/biodiv/d140101

Species diversity of Selaginella in Mount Lawu, Java, Indonesia AHMAD DWI SETYAWAN1,2,♥, SUTARNO1,3, SUGIYARTO1,3 1

Department of Biology, Faculty of Mathematics and Natural Sciences, Sebelas Maret University. Jl. Ir. Sutami 36A Surakarta 57126, Central Java, Indonesia. Phone/Fax. +62-271-663375, email: volatileoils@gmail.com 2 Program of Conservation Biology, Department of Biology, Faculty of Mathematics and Natural Sciences, University of Indonesia, Depok 16424, West Java, Indonesia 3 Program of Bioscience, School of Graduates, Sebelas Maret University. Surakarta 57126, Central Java, Indonesia Manuscript received: 2 April 2013. Revision accepted: 17 April 2013.

ABSTRACT Setyawan AD, Sutarno, Sugiyarto. 2013. Species diversity of Selaginella in Mount Lawu, Java, Indonesia. Biodiversitas 14: 1-9. Selaginella is a genus of ferns allies that lives in moist areas and requires water for fertilization; therefore it is often found in highlands. The aim of this research was to know species diversity of Selaginella in Mount Lawu and the vicinity areas. The research was conducted between July 2007 and November 2012 on the western and southern slopes of Mount Lawu, Central- and East-Java, Indonesia, with altitudes between 1100 and 2100 m a.s.l. The research included three sites and the vicinity areas, i.e. (i) Protected forest of Cemorosewu, (ii) Grojogansewu Natural Recreation Park, and (iii) KGPAA Mangkunagoro I (Ngargoyoso) Grand Forest Park. The research found nine selaginellas species, namely: S. aristata, S. ciliaris, S. involvens, S. opaca, S. ornata, S. plana, S. remotifolia, S. singalanensis and S. zollingeriana. Key words: species, diversity, taxonomy, Mount Lawu, Java

INTRODUCTION Mount Lawu, or Gunung Lawu, is a massive compound stratovolcano, straddling the border between Central Java and East Java, Indonesia (Lat: 7.625°S, Long: 111.192°E). The north side is deeply eroded and the eastern side contains parasitic crater lakes and parasitic cones. Mount Lawu has long been inactive, but still shows volcanic activity, where there is a fumarolic area on the south flank at 2,550 m. The only reported activity of Mount Lawu took place in 1885, when rumblings and light volcanic ash falls were reported (GVP 2012). Geologically, the mountain is divided into two parts, the northern part commonly known as Mount Lawu (3265 m) is the new Lawu, while the southern part known as Jobolarangan Hill (2298 m) is the ancient Lawu (Puslitbang Geologi 1992; Pratiwi 2011). Forest fires regularly occur in Mount Lawu. The latest incident was the destruction of 500 hectares of forest at the end of 2012. Large forest fires also occurred in 2002 (6284.24 ha), 2006 (1007 ha) and 2009 (1370.7 ha) (Beritasatu 25/09/2012; Tribunnews 26/09/2012). Protected forest area in Mount Lawu is approximately 20,400 ha (Sriyanto 2003) or 24,188 ha (BLI 2004). The main area of the forest is managed by Lawu DS Forest Management Unit (consisting of North Lawu: 5354.7 ha and South Lawu: 5719.4 ha), and the rest is managed by Surakarta Forest Management Unit (Kesatuan Pengelolaan Hutan; KPH). There are two nature conservation areas in the mountain, namely: Grojogansewu Natural Recreation Park (Taman Wisata Alam; TWA) established by the Ministry of Agriculture decree No. 264/Kpts-Um/10/1968 dated October 12, 1968 covering an area of 64.30 ha; and

KGPAA Mangkunagoro I Grand Forest Park (formerly Ngargoyoso Grand Forest Park; Taman Hutan Raya (Tahura) Ngargoyoso) established by the Ministry of Forestry and Plantations decree No. 849/Kpts-II/1999 dated October 11, 1999 covering an area of 231.3 ha. At this time, grand forest park is proposed to be expanded to reach approximately 1000 ha, covering Karanganyar and Wonogiri, Central Java (Slamet, Office of Forestry, Central Java Province, 2012, pers. com.). Mount Lawu has an important function for the protection of natural resources and ecosystems. This area is a buffer zone that limits the distribution of dry-type ecosystems in eastern Java and wet-type ecosystem in western Java. Mount Lawu is one of the western distribution borders of Casuarina junghuhniana Miq. (Pinyopusarerk and Boland 1995), and of the eastern distribution borders of Schima wallichii (DC.) Korth., although this later species is probably non-native in Mount Lawu (Steenis 1972). Several studies on plant diversity in Mount Lawu have been conducted, for example: fungi (Ilyas 2007), cryptogamae (Setyawan and Sugiyarto 2001), spermatophytes (Sutarno et al. 2001), epiphytic plants (Setyawan 2000), epiphytic orchids (Marsusi 2001; Yulia et al. 2011), epiphytic medicinal plants (Samsali 2008), fruit plants Rubus (Setyawan 1999), medicinal herb Plantago major (Sugiyarto et al. 2006), Vanda tricolor orchid (Suparno-Putri 2013), home-garden plants (Harsono 2001), plants of Cemorosewu (Khussurur 2006), etc. This region has been proposed as a national park (Setyawan and Sutarno 2000; Setyawan 2001; Sriyanto 2003; Setyawan and Dirgahayu 2005; WDPA 2010).

B I O D I V E R S IT A S 14 (1): 1-9, April 2013

Selaginella is one of the genera that live in Mount Lawu. This plant lives in moist environment and requires water for fertilization. Mountainous region with humid climate and abundant water sources throughout the year is a hotspot for its diversity. Research on species diversity of Selaginella in Mount Lawu had never been conducted before, but there have been reports of the presence of S. ornata (Setyawan and Sugiyarto 2001) and S. opaca (Setyawan 2009). The observation on the Herbarium Bogoriense (BO) collections have found three Selaginella species of Mount Lawu, namely: S. aristata, S. opaca, and S. involvens (ADS 2012, pers. obs.). A large number of Selaginella species are morphologically polymorphic and have high morphological similarity among species; Selaginella is a difficult genus to be classified (Setyawan et al. 2012). This confusion led to almost every species having more than one name, even S. ornata and S. involvens, which have high morphological variation, each having more than 25 synonyms (Kessler and Swale 2008). Nowadays, there are 700-750 recognized species around the world, while more than 200 species are found in Nusantara (Malay Archipelago), 25 species in Java (Setyawan 2008), 10 species in southern Central Java (Setyawan 2012) and eight species in Mount Merapi, Java (Setyawan et al. 2012). Since Selaginella commonly grows well in humid places and requires water for fertilization, it becomes interesting for studying the biodiversity and the climate change. This study aimed to determine the diversity of Selaginella in Mount Lawu and the surrounding areas.

MATERIALS AND METHODS The field work was carried out more than six years, between July 2007 and November 2012. Several surveys of Selaginella have been conducted in Mount Lawu and the adjacent areas, with altitude between 1100 and 2100 m a.s.l., both in the wet and dry seasons. The research sites were grouped into three divisions, namely: (i) Protected forest of Cemorosewu (1600-2100 m a.s.l.), (ii) Grojogansewu Natural Recreation Park (1100-1400 m a.s.l.), and (iii) KGPAA Mangkunagoro I (Ngargoyoso) Grand Forest Park (1100-1500 m a.s.l.). Survey sites indicating the presence of Selaginella was shown in Table 1 and Figure 1. All three sites are influenced by human activities. Selaginella is generally found in places that are moist and shady, such as roadside cliffs, footpaths and tributries cliffs. Some species can also grow in relatively open sites, such as forest stands of pine (Pinus merkusii), the settlements and agricultural land. Selaginella rarely grows under a dense clumps of herbs or shrubs; that place does not provide space and light for growth. The southern and western slopes of Mount Lawu – where this research was conducted – has Andisol soil type (Sargiman 1990; Sarifuddin 1998; Jubaedah 2008). This clay soil type has relatively higher ability to hold water and nutrients than pyroclastic sandy soil in the northern and eastern slopes. All Selaginella species were recorded and collected as herbarium specimen and living collection for the experimental garden in Kejiwan, Wonosobo, Central Java

Table 1. Study sites of Selaginella diversity and distribution in Mount Lawu and the adjacent areas. Sites*

Latitude

Longitude

Altitude (m)

Protected forest of Cemorosewu and the vicinity (1600-2100 m) Cemorokandang -7.665113° 111.181350° Cemorosewu-1 -7.656752° 111.195046° Cemorosewu-2 -7.667108° 111.191757° Cemorosewu-3 -7.670575° 111.193019° Cemorosewu-4 -7.664144° 111.197845° Cemorosewu-5 -7.666296° 111.196120° Jobolarangan-1 -7.668915° 111.190381° Jobolarangan-2 -7.684914° 111.182679° Jobolarangan-3 -7.670727° 111.182348°

1807 2070 1876 1633 1915 1865 1754 1884 1753

Natural Recreation Park of Grojogansewu and the vicinity (1100-1400 m) Blumbang-1 -7.664726° 111.155295° 1382 Blumbang-2 -7.670324° 111.158458° 1464 Kalisoro -7.663311° 111.152281° 1337 Tawangmangu-1 -7.661767° 111.143464° 1222 Tawangmangu-2 -7.660820° 111.136199° 1133 Tawangmangu-3 -7.660554° 111.139010° 1150

Species diversity S. opaca, S. remotifolia S. opaca, S. remotifolia S. opaca S. opaca S. opaca, S. remotifolia S. remotifolia S. opaca S. opaca S. opaca, S. remotifolia S. involvens, S. opaca, S. ornata, S. remotifolia S. remotifolia S. remotifolia S. zollingeriana S. zollingeriana S. aristata, S. ciliaris, S. involvens, S. opaca, S. ornata, S. plana, S. remotifolia, S. singalanensis

Grand Forest Park of KGPAA Mangkunagoro I (Ngargoyoso) and the vicinity (1100-1500 m) Kemuning -7.597704° 111.139299° 1156 S. remotifolia Nglerak -7.608175° 111.154545° 1556 S. remotifolia Tahura Ngargoyoso -7.626599° 111.133633° 1220 S. aristata, S. ciliaris, S. opaca, S. remotifolia, S. singalanensis, S. zollingeriana Note: *) Each site is the midpoint of the few locations in the surrounding

SETYAWAN et al. â&#x20AC;&#x201C; Selaginella of Mount Lawu, Java

NGAWI

KARANGANYAR

MAGETAN

WONOGIRI

A B

Figure 1. Study sites of Selaginella diversity in Mount Lawu ( ): A. Cemorosewu Protected Forest and the vicinity, B. Grojogansewu Natural Recreation Park and the vicinity, C. KGPAA Mangkunagoro I (Ngargoyoso) Grand Forest Park and the vicinity. Insert: Mount Lawu Protected Forest (Âą 20,400 ha).

(768 m a.s.l.). A total of 56 herbarium specimens of nine species of Selaginella have been collected from the study site (Table 1). Each herbarium specimen was unique, distinguished by location and time of collection. Data passport collected along with the specimens were used as standard for herbaria specimen. The specimens were identified by using several literatures on selaginellas, i.e. Alderwereld van Rosenburgh (1915a,b, 1916, 1917, 1918, 1920, 1922) and Alston (1934a, 1935a,b, 1937, 1940); and were compared with the specimens collection at BO, especially the specimens that had been determined by A.G.H. Alston before; and also by using several newest references such as Wong (1982, 2010), Tsai and Shieh (1994), Li and Tan (2005), and Chang et al. (2012). In addition to direct observations, we use the literatures to guide the preparation of the description. Meanwhile, the global distribution is according to Hassler and Swale (2002).

RESULTS AND DISCUSSION Description Selaginella is an annual (S. aristata, S. ciliaris, S. zollingeriana) or perennial herb. Stems are leafy, slender, descending (S. aristata), creeping and rooting at intervals

(S. ciliaris, S. opaca, S. remotifolia, S. singalanensis), ascending (S. aristata, S. plana), or erect, without branches on lower part, rooting near base, roll up when dry (S. involvens), branching dichotomously, regularly or irregularly branched. Rhizophores are present or absent (S. involvens), geotropic, borne on stems at branch forks, throughout (creeping ones), or confined to base (S. ornata). Leaves are small, simple, with a single vein (rarely veins forked), always bearing an inconspicuous ligule on the adaxial side at its base (only prominent in early development); vegetative leaves are (tropophyll) monomorphic-spirally arranged at basal main stem and dimorphic-4 lanes arranged on other parts (S. involvens, S. plana), or more often dimorphic and usually arranged in two median (ventral) and two lateral (dorsal) rows on the branches (S. ornata, S. singalanensis); median leaves are usually smaller, and in different shape from the lateral leaves; axillary leaves are single borne at the forking of each branch, being somewhat different from other leaves. Strobilus (clusters of imbricating sporophylls) are usually borne on the ends and sides of branches, cylindric, tetragonal (S. involvens, S. opaca, S. remotifolia), flattened (S. ciliaris) or do not in compact strobilus (S. aristata, sometimes). Sporophylls (fertile leaves) are monomorphic or adjacently different, slightly or highly differentiated from vegetative leaves. Sporangia are short-stalked,

B I O D I V E R S IT A S 14 (1): 1-9, April 2013

solitary in an axil of sporophylls, opening by distal slits. Spores are of two types (heterosporous), megaspores tetrad (1-2-)4, large, commonly at the base of strobilus, microspores numerous (hundreds), minute; sporangia round or oval, opening by a transverse slit. Selaginellaceae Reinch. is a family with only one genus namely Selaginella P. Beauv., cosmopolitan fern allies, consisting of about 700-750 species; 200s species in Nusantara, 25 species in Java, and nine species in Mount Lawu (Table 2). The results indicated that - at an altitude of 1100 to 2100 m - getting to the top, the number of collected Selaginella species decreased (Table 2). This suggests that the distribution of Selaginella is affected by altitude. A total of 9 species were found in Grojogansewu (1100-1400 m), 6 species in Ngargoyoso (1100-1500 m), and only two species in Cemorosewu (1600-2100 m). Altitude of 2100 m seems to be the upper limit of Selaginella distribution; therefore it is very interesting to conduct similar research at an altitude below 1100 m, and to know the distribution shift of Selaginella from the coastal area to the summit of Mount Lawu. Besides, a large number of species found in Grojogansewu are also allegedly associated with the local physiography. This area has a lot of high cliffs and small rivers, making it very suitable for the growth of Selaginella. In Java, the altitude of 1500 m may be the upper limit for the spread of S. aristata, S. ciliaris, S. involvens, S. ornata, S. plana, S. singalanensis, and S. zollingeriana. Meanwhile, the altitude of 2100 m is probably the upper limit for the spread of S. opaca and S. remotifolia.

S. aristata S. ciliaris S. involvens S. opaca S. ornata S. plana S. remotifolia S. singalanensis S. zollingeriana Total

● ● ● ● ● ● ● ● ● 9

● ● ●

●

● ● ● 6

●

Total herbaria speciment

Cemorosewu (1600-2100 m)

KGPAA Mangkunagoro I (Ngargoyoso) (1100-1500 m)

Species

Grojogansewu (1100-1400 m)

Table 2. Species diversity and distribution of Selaginella in Mount Lawu and the adjacent areas.

4 4 4 16 3 3 14 4 4 56

Note: Each herbarium specimen was unique, distinguished by location and/or time of collection.

Key to species 1. Stem (sub-)erect, rooting at base, or bearing rhizophores ........................................................................................... 2

2. Stem shorter than 30 cm ........................................... 3. Stem fleshy ...................................... S. aristata 3. Stem fragile ...................................... S. ornata 2. Stem longer than 30 cm ........................................... 4. Stem hard, caulescent, easily broken .............. ......................................................... S. involvens 4. Stem tough ......................................... S. plana 1. Stem creeping, rooting at intervals .............…..…….…… 5. Stem shorter than 15 cm ........................................... 6. Leaves ovate to rounded ...................... S. ciliaris 6. Leaves lanceolate ....................... S. zollingeriana 5. Stem more than 15 cm ............................................. 7. Stem fleshy .......................................... S. opaca 7. Not so ................................................................ 9. Leaves loosely arranged ......... S. remotifolia 9. Leaves imbricate ............... S. singalanensis

5 6

7 8

Species description Selaginella aristata Spring; Bull. Acad. Brux. 10: 232, no. 152 (1843) (Figure 2A) It is a small, fleshy, annual herb, prostrate to ascending, caespitose, fan-shaped; multiple branched at main stem, every branch forming dendritic stem. Stems are decumbent to ascending, dendritic branched, especially at the mature ones, ca. 4-20 cm long, 3-6 mm wide (including leaves). Rhizophores are present at basal stem, originated from the ventral side of branching stem, ca. 1 mm in diam. Leaves (trophophylls) are dimorphic, arranged in 4 lanes (2 lateral, 2 median), loosely arranged at the main stem but closely arranged at the branches, vein single; lateral leaves are lanceolate to oblong-ovate at main stem, lanceolate to falcate at branches, 1.8-3 mm long, 1-2 mm wide, base subcordate or rounded, asymmetrical, apex acute or obtuse, margin serrulate to subentire; median leaves are smaller than the lateral ones, lanceolate to ovate, more or less symmetrically, 1.2-2 mm long, 0.5-1 mm wide, base obtuse, apex caudate to long tail-like, apices are upward or bended back, margin serrulate, single vein reaching the apex; axillary leaves are lanceolate to ovate, 1.5-3 mm long, 0.5-1.5 mm wide, single vein nearly reaching the apex, base rounded, apex obtuse, margin serrulate. Strobilus are solitary, terminal, loosely, bisymmetrical, upper-plane sporophylls longer than lower-plane, ovate, complanate, apex acute, pointing outwards, up to 1 cm long. Locality: Grojogansewu, Ngargoyoso Habitat and ecology: it was found on steep cliffs, at the edge of the ditch/irigation water, and up to the stream that flows into Grojogansewu waterfall. It was also found on the cliff edge of the dirt- and cemented road to the Tahura office shaded by pine and secondary forest, only abundant in the rainy season, at altitude of 1150-1220 m a.s.l. Distribution: Myanmar (Burma), Java, Sulawesi, Ternate, Philippines Selaginella ciliaris (Retz.) Spring; Bull. Acad. Brux. 10: 23 (1843) (Figure 2B) It is a small, annual herb, creeping or ascending, sometimes fan-shaped, 4-15 cm in size. Stems are recumbent, without a significant main stem, 4-5 mm wide (including leaves). Rhizophores are present at intervals but

SETYAWAN et al. â&#x20AC;&#x201C; Selaginella of Mount Lawu, Java

mostly near the base, originated from the lateral side of branching stem, ca. 0.3 mm in diam. Leaves are dimorphic, arranged in 4 lanes (2 lateral, 2 median), vein single; lateral leaves are ovate-lanceolate, more or less symmetrical, 1.5-2 mm long, 0.6-1 mm wide, base rounded or subcordate, apex acuminate or acute, margin serrulate or ciliate, single vein reaching the apex, keeled, pointing outwards; median leaves are ovate to falcate, asymmetrical, 2-2.5 mm long, 0.6-1.5 mm wide, base rounded, apex acute, attenuate or cuspidate, margin serrulate but laciniate at basal part, pointing upwards, minutely toothed, ciliate, midrib prominent, single vein reaching or nearly reaching the apex; axillary leaves are lanceolate to ovate, equally sided (bisymmetrically), 1.8-2.5 mm long, 1-1.5 mm wide, single vein reaching or nearly reaching the apex, base rounded to subcordate, ciliate, apex acute, margin toothed, laciniate at basal part and serrulate at apical part. Strobilus are solitary or twin, terminal, flattened, complanate, up to ca. 1.5-2 cm long;

Locality: Grojogansewu, Ngargoyoso Habitat and ecology: It was found on the steep cliff, at the edge of the irigation water, and up to the stream that flows into Grojogansewu waterfall. It was also found on the cliff edge of the cemented road to the Tahura office shaded by pine and secondary forest, not recorded in the dry season, at altitude of 1150-1220 m a.s.l. Distribution: India, Sri Lanka, Myanmar, S-China (Guangdong), Taiwan, Thailand, Vietnam, New Guinea, Solomons, Java, Sulawesi, Ternate, Philippines, Northern Australia, Marianas, Palau Isl., Micronesia Selaginella involvens (Sw.) Spring; Bull. Acad. Brux. 10: 136, no. 6 (1843) (Figure 2C) It is a robust perennial herb, erect with stoloniferous rhizome, without branches on the lower half, from a very widely creeping shallow subterranean branching rhizome to

Figure 2. Species diversity of selaginellas in Mount Lawu and the surrounding; A. S. aristata, B. S. ciliaris, C. S. involvens, D. S. opaca, E. S. ornata, F. S. plana, G. S. remotifolia, H. S. singalanensis, and I. S. zollingeriana.

B I O D I V E R S IT A S 14 (1): 1-9, April 2013

an ascending rhizome, up to ca. 50 cm tall, 3-4 cm wide (including leaves). It has two types of stems: creeping (rhizome) and erect, with a significant main stem when erect; creeping stems when subterranean. Leaves are monomorphic, colorless, scales ovate ciliate, sessile, apex acute, apprised or recurved; erect branches dendritic, fanshaped, up to more than 40-50 cm long, 1-1.5 mm in diam., with several dormant buds or leaves on lower part of main stem, monomorphic but dimorphic on much branching parts. Rhizophores are absent. Leaves of the basal main stem are monomorphic, ovate, clasping, nearly asymmetrical, appressed, 1-2 mm long, 1-1.8 mm wide, apex acute to attenuate, base truncate, auriculate or not, margin serrate to serrulate but lacerate with spinose at the auricule, arose and long ciliate towards apex. Leaves on the branches are dimorphic, arranged in 4 lanes (2 lateral, 2 median), vein single, reaching the apex; lateral leaves are lanceolate to ovate, asymmetrical, 0.8-2.5 mm long, 0.3-1.5 mm wide, ciliate near base, base oblique with auriculate, apex attenuate or acuminate, vein single always curved and pointing to abaxial side, having 2 significant grooves beside the vein, adaxial blade raised and forming twomain-vein, margin laciniate but spinose at the auricule; median leaves are ovate on the main stem but elliptical or laceolate to ovate on the top branch, asymmetrical, 1.5-3 mm long, 1-2.5 mm wide, base rounded to subcordate, twisting to form miniature auricle at the base, apex acute, single vein, obscure, 1-2 longitudinal groove(s) at the adaxial surface beside the vein of median leaves on the top branch, having 2-3 grooves at the abaxial surface on the top branch, 2 beside the vein and 1, less significant or absent, inside the midrib, margin entire to serrate, laciniate at most basal part of margin, concentrated spinose at the miniatureauricle base, minutely ciliate, pointing upwards; axillary leaves are ovate to cordate on first forked site but lanceolate to ovate at following forked site, asymmetrical, 1-2.5 mm long, 0.5-2.5 mm wide, base subcordate or cordate, apex acute or attenuate, margin serrate but laciniate at basal part, minutely ciliate. Strobilus are solitary, terminal, tetragonal, up to more than 2 cm long. Locality: Grojogansewu Habitat and ecology: It was found on the steep cliff, at the edge of the irigation water and small stream, at altitude of 1150-1382 m a.s.l. Distribution: India, Bhutan, Nepal, Sri Lanka, Myanmar, China, Japan, Ryukyu Isl., Korea, Vietnam, Laos, Cambodia, Thailand, Java, Kalimantan, Sulawesi, Flores, Palau Isl. Selaginella opaca Warb.; Monsunia 1: 108, 122, no. 112 (1900) (Figure 2D) It is a fleshy herb, perennial. Stems are creeping to ascending, usually fertile branches alternate on long fleshy main stem, up to 80 cm long, 3-8 cm wide (including leaves). Rhizophores are at the branching stem, mostly near the base, originated from the dorsal side of stem at the branch site, ca. 1-1.5 mm in diam. Leaves on the main stem are monomorphic, oblong, asymmetrical, spaced farther apart than their width, midrib present. Leaves on the branches are dimorphic, arranged in 4 lanes (2 dorsal, 2

ventral), loosely arranged at long creeping stem but closely arranged at branches; lateral leaves are ovate to oblong, asymmetrical, 2-5 mm long, 2-3 mm wide, base rounded, apex acute, vein single, obscure, not reaching the apex, margin serrulate to entire or minutely ciliate at the base, pointing outwards, imbricating at the ends of branches; median leaves are ovate to oblong, asymmetrical, 1.5-3 mm long, 1-2 mm wide, base obliquely cordate or cordate, apex caudate, pointing upwards, imbricating at the ends of branches, vein single not reaching the apex, margin serrulate or serrate, but entire at basal part; axillary leaves are ovate, entire, rounded or obtuse, symmetrical, 2.5-3.5 mm long, 1.5-2.5 mm wide, apex acute, margin entire or serrulate at apical part. Strobilus are solitary, terminal or lateral, tetragonal, up to more than 3.5 cm long. Locality: Grojogansewu, Ngargoyoso, Cemorosewu Habitat and ecology: It was found on the steep cliffs and river bank above the channel irrigation and small river to Grojogansewu waterfall, on the cliff at the edge of the dirt-road and cemented road to the Tahura office shaded by pine and secondary forest, on the cliffs on the river banks near the bridge and new highway, along the footpath and the cliffs from Cemorosewu to Grojogan kembar waterfall, on the edge of several small springs near the camping ground, on the small tributaries in Jobolarangan Hills, on the cliff above the old road of Cemorokandang to Sarangan, on the trekking lane above Cemorosewu, near the field that made after forest fire. It could be found throughout the year; at altitude of 1150-2070 m a.s.l. This species is mostly found near S. remotifolia Distribution: Sumatra, Java, Lombok, Ceram, New Guinea, Philippines Selaginella ornata (Hook & Grev.) Spring; Bull. Acad. Brux. 10: 232 (1843) (Figure 2E) It is a fragile perennial herb, greenish or brownish in general appearance. Stems are suberect fragile, very easily broken, 20-30 cm long, 1-3 cm wide (including leaves). Rhizophores are at the lower part and sometimes at branching stem, originated from the dorsal side of stem at the branch site, ca. 0.5-1 mm in diam. Leaves are dimorphic, arranged in 4 lanes (2 dorsal, 2 ventral), densely arranged throughout the stem and imbricating at top of branches; lateral leaves are oblong to falcate, denticulate to dentate, exauriculate, asymmetrical, 1.5-3 mm long, 1-1.5 mm wide, apex acuminate to acute, and prickly tip, vein single not reaching the apex, base rounded to truncate, margin entire; median leaves are denticulate to dentate, with arista often more than half the lamina length, asymmetrical, 1-1.5 mm long, 0.5-1 mm wide, apex acute, prickly tip, base rounded, vein single not reaching the apex, margin entire; axillary leaves are ovate to subcordate, exauriculate, imbricating, asymmetrical, 1-1.5 mm long, 0.51 mm wide, apex acute, base rounded, margin entire. Strobilus are solitary, terminal, bisymmetrical, upper-plane, up to more than 1 cm long. Locality: Grojogansewu Habitat and ecology: It was found the steep cliffs above a small irigation channel and tributary of Grojogansewu waterfall, on the cliffs on the small river banks near the

SETYAWAN et al. â&#x20AC;&#x201C; Selaginella of Mount Lawu, Java

bridge and new highway; at altitude of 1150-1382 m a.s.l. Distribution: India, Thailand, Vietnam, Cambodia, Peninsular Malaysia, Sumatra, Java, Kalimantan, Bali, Lombok, Flores, Philippines Selaginella plana (Desv. ex Poir.) Hieron.; Nat. Pflanzenfam. 1 (4): 703 (1901) (Figure 2F) It is a stout perennial herb. Stems are sub-erect with stoloniferous rhizome, without branches on the lower part, ascending from a subterranean trailing base, up to 80-100 cm long, 3-10 cm wide (including leaves); subterranean stems (rhizome) shallowly radiating. Rhizophores are sometimes at the branching stem, originated from the dorsal side of stem at the branch site, ca. 1-1.5 mm in diam. Leaves on the lower part and main stem are monomorphic, well spaced, appressed, 1.5-3 mm long, 1-2 mm wide, upper part slightly spreading, ovate, apex acuminate or acute, but rounded tip, asymmetrical, margin translucent, entire. Leaves on the branches are dimorphic, arranged in 4 lanes (2 dorsal, 2 ventral), loosely arranged at lower stem but closely arranged at branches; lateral leaves are oblong to ovate, asymmetrical, 2-4.5 mm long, 2-3 mm wide, apex acuminate to acute, but rounded tip, sessile, vein single, obscure, not reaching the apex, base truncate and rounded, upper base with a spur-like lobe which overlaps the stem, margin transparent, entire; median leaves are ovate to oblong, asymmetrical, 1.5-3 mm long, 1-2 mm wide, apex acuminate to acute, but rounded tip, sessile, vein single, obscure not reaching the apex, base truncate and rounded, margin transparent, entire; axillary leaves are ovate, asymmetrical, 2.5-3.5 mm long, 1.5-2.5 mm wide, apex acute, minutely ciliate, base rounded, margin entire. Strobilus are solitary, terminal, tetragonal, up to more than 3 cm long. Locality: Grojogansewu Habitat and ecology: It was found on the steep cliffs above a small irrigation channel and tributary of Grojogansewu, remaining abundant in the dry season, altitude 1150 m a.s.l. Notes: It is originally low-lying vegetation, and 1200 m altitude in Turgo (Mt. Merapi) is probably the highest point that species can reach in Java (Setyawan et al. 2012). Distribution: Peninsular Malaysia, Sumatra, Java, Bali, Timor, Flores, Sumbawa, Solor, Sulawesi, Maluku (Ambon, Banda, Ceram, Kei Isl., Ternate, Buru). Introduced: India, Taiwan, Philippines, Florida, Puerto Rico, Honduras, Costa Rica, Panama, Colombia, Brazil, Jamaica, Trinidad, St. Kitts, Barbados, Ecuador, British Guyana, St. Thomas, Dominica, Martinique, Tanzania. Selaginella remotifolia Spring; Miq. Pl. Jungh. 3: 276, no. 5 (1854) (Figure 2G) It is a wiry, perennial herb. Stems are creeping, usually several fertile branches alternate on long main stem, up to 100 cm long, 0.5-1 cm wide (including leaves). Rhizophores are at the branching stem, originated from the dorsal side of stem at the branch site, ca. 0.5 mm in diam. Leaves are on the main stem monomorphic, lanceolate, acuminate, asymmetrical, spaced farther apart than their width, midrib present. Leaves on the branches are dimorphic, arranged in 4 lanes (2 dorsal, 2 ventral), loosely

arranged at the long creeping main stem but closely arranged at branches; lateral leaves are contiguous, lanceolate to ovate, asymmetrical, 1.5-3 mm long, 1-2 mm wide, apex acute to acuminate, vein single, obscure not reaching the apex, base rounded, margin serrulate but usually entire or minutely ciliate, pointing outwards; . median leaves are lanceolate to ovate, asymmetrical, 1.52.5 mm long, 0.5-1 mm wide, base obliquely cordate or cordate or cuneate, apex attenuate or caudate, leaves at ends of branches imbricating, vein single not reaching the apex, margin serrulate or serrate, but entire at abaxial medium and basal part; axillary leaves are ovate, entire, rounded or obtuse, symmetrical, 2-2.5 mm long, 1-1.5 mm wide, apex acute, margin entire or loosely serrulate at apical part. Strobilus are solitary, terminal or lateral, tetragonal, up to more than 2 cm long. Locality: Grojogansewu, Ngargoyoso, Cemorosewu Habitat and ecology: It was found on the steep cliffs and river bank above the channel irrigation and small river towards Grojogansewu waterfall, on the cliff at the edge of the dirt-road and cemented road to the Tahura office shaded by pine and secondary forest, among pine stand of Tahura forest, on the cliffs on the river banks near the bridge and new highway, and around the vegetable fields, along the footpath and cliffs from Cemorosewu to Grojogan Kembar waterfall, on the edge of several small springs near the camping ground, cliff above the old road of Cemorokandang to Sarangan, on the trekking lane above Cemorosewu, near the field made after forest fire. It grew throughout the year but decreased at dry season; at altitude of 1150-2070 m a.s.l. Distribution: Myanmar, China (Guizhou, Guangxi, Yunnan), Taiwan, Japan, Ryukyu Isl., Korea, Sumatra, Java, New Guinea, Philippines Selaginella singalanensis Hieron.; Hedwigia 50: 18, no. 12 (1910) (Figure 2H) It is a tender, perennial herb, in humid environments, growing all year round, yellowish in general appearance. Stems are creeping, attached to the ground, very soft and very thin, 20-25 cm long, 1-3 cm wide (including leaves). Rhizophores are at branching stem, originated from the dorsal side of stem at the branch site, ca. 0.5 mm in diam. Leaves are dimorphic, very soft, arranged in 4 lanes (2 dorsal, 2 ventral), densely arranged at thorough stem and imbricating at top of branches; lateral leaves are oblong, imbricating, asymmetrical, 1.5-2.5 mm long, 0.5-1.5 mm wide, apex acute, vein single not reaching the apex, base rounded, margin entire; median leaves are dentate, exauriculate, asymmetrical, 0.5-1.5 mm long, 0.5 mm wide, apex acute, vein single not reaching the apex, base rounded, margin entire; axillary leaves are ovate, imbricating, asymmetrical, 0.5-1.5 mm long, 0.5 mm wide, apex acute, base rounded, margin entire. Strobilus are solitary, terminal, loosely, bisymmetrical, upper-plane, up to more than 1 cm long. Locality: Grojogansewu, Habitat and ecology: It was found on the steep cliffs and river bank above the channel irrigation and small river towards Grojogansewu waterfall, on the cliff at the edge of

B I O D I V E R S IT A S 14 (1): 1-9, April 2013

the cemented road to the Tahura office shaded by pine and secondary forest. It generally died in the dry season, but in a moist area it could grow throughout the year; at altitude of 1150 m a.s.l. Distribution: Sumatra, Java Selaginella zollingeriana Spring; Miq., Fl. Jungh. 3: 278, no. 11 (1854) (Figure 2I) It is a slender annual herb, annual, ascending, fanshaped; multiple branched at main stem, every branch forming dendritic stem. Stems are ascending, dendritic branched, especially at the mature ones, ca. 5-15 cm long, 3-5 mm wide (including leaves). Rhizophores are only present at lower part, ca. 0.5 mm in diam. Leaves on the main stem are monomorphic, lanceolate, acuminate, asymmetrical, spaced farther apart than their width. Leaves on the branches are dimorphic, arranged in 4 (2 lateral, 2 median), loosely arranged at the main stem but closely arranged at the top branches, vein single; lateral leaves are lanceolate, asymmetrical, 1.5-2 mm long, 0.5-1.5 mm wide, apex acute, base rounded, margin entire; median leaves are smaller than lateral ones, lanceolate, 1-1.5 mm long, 0.5 mm wide, apex caudate to long tail-like, margin entire, single vein; axillary leaves are lanceolate to subcordate, ca 1-1.5 mm long, 0.5-1 mm wide, single vein nearly reaching the apex, apex acute, base rounded, margin entire. Strobilus are solitary, loosely, bisymmetrical, upper-plane, up to ca. 1 cm long. Locality: Grojogansewu, Ngargoyoso, Habitat and ecology: It was found on the cliff walls of the tomb and headstone, on the cliff at the edge of the cemented road to Tahura office shaded by pine and secondary forest, on the roadside on the plastered and dirt drainage ditch; not recorded in the dry season, at altitude of 1150-1222 m a.s.l. Distribution: Bali, Java

CONCLUSION Nine species of selaginellas have been found in Mount Lawu and the adjacent areas, namely: S. aristata, S. ciliaris, S. involvens, S. opaca, S. ornata, S. plana, S. remotifolia, S. singalanensis and S. zollingeriana. All species could be identified based on its vegetativemorphological characteristics.

ACKNOWLEDGEMENTS We thank the head and staff of Herbarium Bogoriense (BO), RCB-IIS, Cibinong-Bogor, Indonesia for facilitated the herbarium materials, the same to the management of Tahura KGPAA Mangkunagoro I Ngargoyoso, TWA Grojogansewu and Perhutani (BKPH Lawu Utara). Parts of this work were supported by Featured Research Higher Education (Decentralization Research Grant) from Directorate General of Higher Education, Ministry of Education and Culture, RI for fiscal year 2013.

REFERENCES Alderwereld van Rosenburgh CRWK van. 1915a. Malayan fern allies. Department of Agriculture, Industry, and Commerce. Batavia. Alderwereld van Rosenburgh CRWK van. 1915b. New or interesting Malay ferns 7. Bull Jard Bot Buitenzorg 2 (20): 1-28. Alderwereld van Rosenburgh CRWK van. 1916. New or interesting Malay ferns 8. Bull Jard Bot Buitenzorg 2 (23): 1-27. Alderwereld van Rosenburgh CRWK van. 1917. New or interesting Malay ferns 9. Bull Jard Bot Buitenzorg 2 (24): 1-8. Alderwereld van Rosenburgh CRWK van. 1918. New or interesting Malay ferns 10. Bull Jard Bot Buitenzorg 2 (28): 1-66. Alderwereld van Rosenburgh CRWK van. 1920. New or interesting Malay ferns 11. Bull Jard Bot Buitenzorg 3 (2): 129-186. Alderwereld van Rosenburgh CRWK van. 1922. New or interesting Malay ferns 12. Bull Jard Bot Buitenzorg 3 (5): 179-240. Alston AHG. 1935a. The Selaginella of the Malay Islands: I. Java and the Lesser Sunda Islands. Bull Jard Bot Buitenzorg 3 (13): 432-442. Alston AHG. 1935b. The Philippines species of Selaginella. Philippines J Sci 58: 359-383. Alston AHG. 1937. The Selaginella of the Malay Islands: II. Sumatra. Bull Jard Bot Buitenzorg 3 (14): 175-186. Alston AHG. 1940. The Selaginella of the Malay Islands: III. Celebes and the Maluku. Bull Jard Bot Buitenzorg 3 (16): 343-350. Alston, AHG. 1934. The genus Selaginella in the Malay Peninsula. Gard Bull Strait Settl 8: 41-62. Beritasatu. 25/09/2012. Hundreds acres of Mount Lawu Forest burned (www.beritasatu.com). [Indonesian] BLI [BirdLife International]. 2004. Im shportant Bird Areas in Asia; Key sites for conservation. BirdLife Conservation Series No. 13. BirdLife International, London. www.birdlife.org Camus G, Gourgaud A, Mossand-Berthommier PC, Vincent PM. 2000. Merapi (Central Java, Indonesia): An outline of the structural and magmatological evolution, with a special emphasis to the major pyroclastic events. J Volcanol Geothermal Res 100 (1-4): 139-163 Chang HM, Chiou WL, Wang JC. 2012. Flora of Taiwan, Selaginellaceae. Endemic Species Research Institute, Nantou, Taiwan. GVP [Global Volcanism Program]. 2012. Lawu. Smithsonian Institution, Washington DC. Harsono S. 2001. Diversity of rural farmer’s homegarden plants association with environmental factors in western slopes of Mount Lawu. [Thesis]. Environmental Science Program, University of Gadjah Mada, Yogyakarta. [Indonesian] Hassler M, Swale B. 2002. Checklist of world ferns on CDROM. http://homepages.caverock.net.nz; bj@caverock.net.nz Ilyas M. 2007. Isolation and identification mould micoflor a inhabiting plant leaf litter from Mount Lawu, Surakarta, Central Java. Biodiversitas 8 (2): 105-110. [Indonesian] Jubaedah. 2008. Relationship beetween amorphous mineral components and physical properties of Andisol from Mount Merbabu and Mount Lawu Central Java. [Thesis]. Soil Science Program, University of Gadjah Mada, Yogyakarta. [Indonesian] Khussurur M. 2006. Identification of plants stand of Cemorosewu forest, Magetan District, East Java [Hon. Thesis]. Department of Forestry, University of Muhammadiyah Malang, Malang. [Indonesian] Li ZJ, Tan BC. 2005. A review of the species diversity of Selaginella in Fujian Province of China. Acta Phytotaxonomica Sinica 43 (1): 50-59 Marsusi, Mukti C, Setiawan Y, Kholidah S, Viviati A. 2001. A Study of the Epiphytic Orchids in Jobolarangan Forest. Biodiversitas 2 (2): 153-158 [Indonesian] Pinyopusarerk KA, Boland DJ. 1995. Casuarina junghuhniana - a highly adaptable tropical casuarina. NFTA 95-01, January 1995. Winrock International, Arkansas, USA Pratiwi EP. 2011. Geology and study of volcano facies of Nglanggran unit, Pohijo area, Sampung sub-district, District of Ponorogo, East Java Province. [Hon. Thesis]. Faculty of Mineral Engineering, Universitas Pembangunan Nasional “Veteran”, Yogyakarta. [Indonesian] Puslitbang Geologi. 1992. Geology map, Ponorogo sheet, Year 1992, Scale 1:100.000. Puslitbang Geologi, Bandung.[Indonesian] Samsali O. 2008. Medicinal epiphytic plants along trecking line of Cemorosewu, Mount Lawu. [Hon. Thesis]. Faculty of Mathematics and Natural Sciences, Sebelas Maret University, Surakarta. [Indonesian]

SETYAWAN et al. – Selaginella of Mount Lawu, Java Sargiman G. 1990. The role of some properties of mineralogy, soil chemistry and physics in the process of structure formation on the western slopes catena of Mount Lawu. [Thesis]. Soil Science Program, University of Gadjah Mada, Yogyakarta. [Indonesian] Sarifuddin. 1998. Study on phosphorus sorption of four soil types from volcanic material of Mount Lawu, Central Java. [Thesis]. Gadjah Mada University, Yogyakarta. [Indonesian] Setyawan AD, Darusman LK. 2008. Review: Biflavonoid compounds of Selaginella Pal. Beauv. and its benefit. Biodiversitas 9 (1): 64-81. [Indonesia] Setyawan AD, Dirgahayu P (eds). 2006. Proceedings of the National Seminar on Mount Lawu Cultural Park, Karanganyar, 16-17 November 2005. RCBB LPPM UNS, Surakarta. [Indonesian] Setyawan AD, Sugiyarto. 2001. Plants biodiversity of Jobolarangan forest Mount Lawu: 1. Cryptogamae. Biodiversitas 2 (1): 115-122. [Indonesian] Setyawan AD, Sutarno (eds). 2000. 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] Setyawan AD. 1999. Distribution and abundance of Rubus in Mount Lawu. BioSMART 1 (2): 35-41. [Indonesian] Setyawan AD. 2000. Epiphytic plants on stand of Schima wallichii (D.C.) Korth. at Mount Lawu. Biodiversitas 1 (1): 14-20. [Indonesian] Setyawan AD. 2001. Review: Possibilities of Mount Lawu to be a National Park. Biodiversitas 2 (2): 163-168. [Indonesian] Setyawan AD. 2008. Species richness and geographical distribution of Malesian Selaginella. 8th Seminary and Congress of Indonesian Plant Taxonomy Association (“PTTI”), Cibinong Science Center, BogorIndonesia, 21-23 October 2008. Sriyanto A. 2003. Conservation of Mount Lawu ecosystem, needs, strategies and future usefulness. Nature Conservation Information

Center, Directorate of Conservation Area, Directorate General of Forest Protection and Nature Conservation, Ministry of Forestry, Jakarta. [Indonesian] Steenis CGGJ van. 1972. The mountain flora of Java. E.J. Brill, Leiden. [Indonesian] Sugiyarto, Setyawan AD, Pitoyo A. 2006. Estimation of abundance and distribution of Plantago major L. in Mount Lawu. Biodiversitas 7 (2): 143-146. [Indonesian] Suparno-Putri B. 2013. Physiological and anatomical responses of vegetative organs of Vanda tricolor Lindl. orchid growing in south slopes of Mount Merapi and western slope of Mount Lawu. [Thesis]. Universitas Gadjah Mada, Yogyakarta. [Indonesian] Sutarno, Setyawan AD, Irianto S, Kusumaningrum A. 2001. Plants biodiversity of Jobolarangan Forest at Mount Lawu: 2. Spermatophyta. Biodiversitas 2 (2): 156-162. [Indonesian] Tribunnews. 26/09/2012. Fire on Mount Lawu fueled by charcoal makers (www.tribunnews.com). [Indonesian] Tsai JL, Shieh WC. 1994. Selaginellaceae. In: Huang TC (ed) Flora of Taiwan. Vol. 1. 2nd ed. Department of Botany, National Taiwan University, Taipei WDPA [World Database on Protected Areas]. 2010. Gunung Lawu Nature Reserve. www.protectedplanet.net Wong KM. 1982. Critical observations on Peninsular Malaysian Selaginella. Gard Bull Sing 35 (2): 107-135 Wong KM. 2010. Selaginellaceae. In Parris BS, Kiew R, Chung RKC, Saw LG, Soepadmo E (eds) Flora of Peninsular4 Malaysia Series 1. Ferns and Lycophytes. Malayan Forest Records No. 48. FRIM Kepong, Selangor. Yulia ND, Budiharta S, Yulistyarini T. 2011. Analysis of epiphytic orchid diversity and its host tree at three gradient of altitudes in Mount Lawu, Java. Biodiversitas 12 (4): 225-228

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 10-16

ISSN: 1412-033X E-ISSN: 2085-4722 DOI: 10.13057/biodiv/d140102

Endophytic fungi associated with Ziziphus species and new records from mountainous area of Oman SAIFELDIN A.F. EL-NAGERABI1, ♥, ABDULQADIR E. ELSHAFIE2, SULEIMAN S. ALKHANJARI1 1

Department of Biological Sciences and Chemistry, College of Arts and Sciences, University of Nizwa, P.O. Box 33, Postal Code 616, Birkat Al Mouz, Nizwa, Oman, Tel. +968 96365052, Fax. +968 25443050, e-mail: nagerabi@unizwa.edu.om 2 Department of Biology, College of Science, Sultan Qaboos University, P.O. Box 36, AlKhoudh, Postal Code 123, Oman Manuscript received: 8 January 2013. Revision accepted: 30 March 2013.

ABSTRACT El-Nagerabi SAF, Elshafie AE, AlKhanjari SS. 2013. Endophytic fungi associated with Ziziphus species from mountainous area of Oman and new records. Biodiversitas 14: 10-16. Ziziphus species of the family Rhamnaceae grow extensively in arid and semi-arid regions. It is possible that the endophytic fungi associated with this plant might enhance the host resistance to the environmental impacts. The endophytic fungal population inhabiting the healthy leaves of Z. spina-christi and Z. hajanensis plants were determined from April 2008 to October 2011. The endophytic fungal communities varied between the two species, and 45 fungal species, 18 sterile mycelia and 12 yeasts were isolated from Z. spina-christi, whereas 35 fungi, 11 sterile mycelia and 5 yeasts were recovered from Z. hajanensis indicating tissue and species-specificity and without any seasonal variation among the endophytes. These endophytes are new to Ziziphus plants and 45 species are new to the mycoflora of Oman, whereas 27 species are new to Arabian Peninsula. The genus Alternaria was the most prevalent (19-81%) followed by Aspergillus (19-78%), Rhizopus stolonifer (78%), Mycelia sterilia (69%), yeasts (47%), Cladosporium (11-56%), Drechslera (14-53%), Curvularia (8-50%), Fusarium (6-33%), Ulocladium (41-31%), Penicillium (3-22%)), Alysidium resinae (11%), Trichocladium (6-11%), Anguillospora longissima, Bactrodesmium rahmii, Catenularia (8%), Helminthosporium sorghi (7%), Dendryphiella infuscans (6%), Hansfordia biophila (3-6%), Arthrinium, Dissophora, and Phoma sorghina (3%). The recovery of many fungal isolates, morphologically various sterile mycelia and yeasts suggests the high biodiversity of the endophytes invading these plants with strong evidence for future isolation of numerous fungal species through adopting more advanced molecular and DNA identification methods. Key words: Al-Jabal Al-Akhdar, biodiversity, endophytic fungi, Oman, species-specificity, tissue-specificity, Ziziphus spina-christi, Z. hajanensis.

INTRODUCTION Mountains are an important ecosystem attracting different interests of the world. They cover 24% of the earth surface and support 12% of the world population as an excellent source for water. They are inhabited by diverse flora and fauna (Anon 2008). In Oman, Al-Jabal Al-Akhdar in the Western Hajer mountains (1500 m) is a globally distinguished ecosystem having various climatic conditions and diverse vegetation. It has experienced rapid development which is associated with noticeable climatic changes and vegetation deterioration. The problem is not limited to conspicuous flora and fauna, but extends to fungi and bacteria which depend on higher plants for their survival (Carlile et al. 2001). Ziziphus also known as “Sedra” is an important genus of the family Rhamnaceae found growing extensively in arid and semi-arid regions and represented by 135-170 species (Bhansali 1975; Mathur and Vyas 1995; Maraghni et al. 2010). Of these, only Z. spina-christi (L.) Wild and Z. hajanensis are common species inhabiting Al-Jabal AlAkhdar and are indigenous to Oman with a wide ecological and geographical distribution growing under variety of environmental conditions and depression in deep sandy soil (Maraghni et al. 2010). They are an excellent source of

food, fodder and fuel (Mathur and Vyas 1995). Recently the anti-inflammatory analgesic and antispasmodic activities were reported in rodents (Borgi et al. 2008; Borgi and Chouchane 2009). Numerous and diverse fungi were isolated from the tissues of most parts of terrestrial and aquatic plants specially the leaves as endophytes (Huang et al. 2008). Endophytes are fungi or other microorganisms which spend at least part of their life cycle inside leaf tissues without causing immediate overt negative effect (Far et al. 1989; Elamo et al. 1999; Strobel 2002; Devarajan et al. 2002; Gamboa and Bayman 2006; Arnold 2007; Huang et al. 2008; Liu et al. 2010; Jalgaonwala et al. 2011). However, certain endophytic fungi might promote growth and improve the ecological adaptability of the host by enhancing plant tolerance to environmental stress and resistance to phytopathogens and/or herbivores (Clay and Schardl 2002; Waller et al. 2005; Barrow et al. 2007; Liu et al. 2010; Sun et al. 2011). Therefore, the alteration of beneficial endophytes could lead to the development of new and devastating disease to the host plant (Mmbaga and Sauve 2009). These endophytes produce innumerable and valuable novel secondary metabolites (Strobe 2002). They are an excellent source of a therapeutically important class of metabolites (Pietra 1997).

EL-NAGERABI et al. – Endophytic fungi associated with Ziziphus

Worldwide, many researchers are collecting and isolating fungi from unexplored sites, habitats and substrates, particularly in extreme environmental conditions (Ilyas et al. 2009). However, of all world plants, it seems that only a few species have had their complete complement of endophytes studies (Strobel 2002; Huang et al. 2008). The variations of endophytes are due in part to generic differences among plants and the variations in environmental conditions (Elamo et al. 1999). In Oman, the research carried out until now focused on coprophilous fungi (Gene et al. 1993; Elshafie 2005), mycotoxins and mycotoxigenic moulds (Elshafie and Al-Shally 1998; Elshafie et al. 1999, 2002), nematophagous fungi (Elshafie et al. 2003, 2005), and some plant diseases (Elshafie and Baomer 2001; Al-Bahry et al. 2005). There are few studies on some plant diseases of cultivated crops in different areas of Oman, nonetheless, there is no single study on the biodiversity of the fungal flora of the wild and cultivated plants of Al-Jabal Al-Akhdar . It is evident that endophytes are among a poorly understood group of fungi (Gazis and Chaverri 2010). It is quite promising to explore interesting endophytic fungal species among the myriad plants including the main two species of the genus Ziziphus namely Z. spina-christi, and Z. hajanensis which have never been explored so far. Therefore, in the present study, the diversity of the endophytic fungi associated with Z. Spina-christi and Z. hajanensis were investigated during the growing seasons, between April 2008 and October 2011, in the mountain of Al-Jabal Al-Akhdar, and the

Figure 1. Sampling site in Al-Jabal Al-Akhdar mountain, Oman.

seasonal variation, biological diversity, and speciesspecificity of these endophytes in the leaves of the two selected plant species were evaluated.

MATERIALS AND METHODS Sampling site This study was carried out in Al-Jabal Al-Akhdar mountain, Oman (Figure 1), which is located at the South of the Arabian Gulf. It is bordered by Yemen on the South, the Arabian Sea on the Southeast, Iran on the Northeast, the United Arab Emirates on the Northwest, and Saudi Arabia on the West. It lays between latitude of 21°00,N - 29°00,N and longitude of 51°00,E - 59°40,E. The climate varies according to variation in geographical regions which is hotdry in the interior, hot-humid in the coastal area and humid in the South with summer monsoon rain. The average temperature is about 26°C with annual precipitation of less than 100 mm (AlKhanjari 2005). Al-Jabal Al-Akhdar in the Western Hajer mountain range above 1500 m with average temperature on the plateau of 18.5°C which is much lower than that in the surrounding region (29°C) and relative humidity of 46%. Plant materials Eighteen samples of healthy green leaves from two different stands of Ziziphus spina-christi and Z. hajanensis

B I O D I V E R S IT A S 14 (1): 10-16, April 2013

were collected at the same elevation of Al-Jabal Al-Akhdar mountain, Oman. The selected plants were identified at the Department of Biological Sciences and Chemistry, College of Arts and Sciences, University of Nizwa, and Department of Biology, College of Science, Sultan Qaboos University. Samples from 10 different plants were collected at different times and seasons between April 2008 to October 20011 (Table 1). The samples were kept in sterile polyethylene bags and stored in refrigerators at 5Â°C to be used for the isolation of the endophytic fungi. Table 1. The collection date and plant material samples used for isolation of endophytic fungi from Ziziphus spina-christi and Z. hajanensis Sample Nos. SM1 SM2 SM3 SM4 SM5 SM6 SM7 SM8 SM9 SM10 SM11 SM12 SM13 SM14 SM15 SM16 SM17 SM18

Tissues used for isolation Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf Green leaf

Sample date 4-2008 6-2008 9-2008 12-2008 3-2009 5-2009 9-2009 11-2009 1-2010 3-2010 5-2010 7-2010 9-2010 12-2010 3-2011 5-2010 7-2010 10-2011

Isolation of endophytic fungi The green leaves of the selected plant were cut into small pieces of 10 mm in length and washed with several changes of sterile distilled water. The pieces were surface disinfected with 70% ethanol for I min followed by 5% sodium hypochlorite for 5 min (Gazis and Chaverri 2010; Liu et al. 2010). The disinfected leaves were aseptically inoculated on Potato Dextrose Agar (PDA, Potato, 200g; dextrose, 20g; agar 15g; distilled water, 1L) supplemented with chloramphenicol (0.05 mg/ml) to inhibit the bacterial growth, until the mycelia appeared surrounding the plant tissues. The inoculated plates were incubated at the ambient temperature (27-29Â°C) for 7-10 days until the mycelial growth was apparent on the media. The fungal colonies which developed on the tissues were then inoculated on Malt Extract Agar (MEA) for preparation of pure colonies and further identification and preservation as dry herbarium materials at the herbaria of Department of Biological Sciences and Chemistry, College of Arts and Sciences, University of Nizwa, and Department of Biology, College of Science, Sultan Qaboos University. Identification of endophytic fungi The isolated endophytic fungi were identified using macroscopic features based upon colony morphology on

the growth media and microscopic observations of mycelia and asexual/sexual spores according to the method described in literature, and consulting many taxonomic books and numerous monographs (Barnett 1955; Raper and Fennell 1965; Kobayashi 1970; Pitt 1979; Ellis 1971, 1976; Sutton 1980; Webster 1980; Nelson et al. 1983; Samson et al. 1995; Barnett and Hunter 1998, 2003; Barac et al. 2004). Data analysis The number of cases of isolation (NCI) of each fungal species was calculated according to modified formula of Gazis and Charerril (2010) as the number of the samples from which the fungus was isolated, whereas the occurrence remarks (OR) as a total number of the samples from which a given species was isolated compared to the total number used for the isolation of the fungi. The number of the samples from which a given species was isolated divided by the total number of the samples was used to calculate the percentage incidence of fungal species in each genus.

RESULTS AND DISCUSSION Biodiversity of endophytic fungi Fifty two species belonging to 21 genera of fungi in addition to unidentified 29 sterile mycelia and 17 yeasts were isolated from the green leaves of two Ziziphus species plants (Z. spina-christi, Z. hajanensis) (Table 2). Of these isolates, 45 species, 18 sterile mycelia and 12 yeasts were isolated form Z. spina-christi, whereas 35 species, 11 sterile mycelia and 5 yeasts were recovered from Z. hajanensis. The highest number of species were recovered from the genus Alternaria (9 species), followed by Drechslera (7 species), Aspergillus and Fusarium (6 species), Cladosporium (4 species), Curvularia, Penicillium (3 species), Hansfordia, Trichocladium, Ulocladium (2 species), and one species of Anguillospora, Bactrodesmium, Catenularia, Dendryphiella, Helminthosporium and Rhizopus along with an unidentified isolates from the genera of Aspergillus, Dissophora, Fusarium, and Penicillium. The species of the genus Alternaria was the most predominant genus on the leaf tissues and were isolated from 19-81% of the samples collected at different time of the year. This genus is followed by Aspergillus (19-78%), Rhizopus stolonifer (78%), sterile mycelia (69%), yeasts (47%), Cladosporium (11-56%), Drechslera (14-53%), Curvularia (8-50%), Fusarium (6-33%), Ulocladium (41-31%), Penicillium (322%)), Alysidium resinae (11%), Trichocladium (6-11%), Anguillospora longissima, Bactrodesmium rahmii, Catenularia (8%), Helminthosporium sorghi (7%), Dendryphiella infuscans (6%), Hansfordia biophila (36%), Arthrinium, Dissophora, and Phoma sorghina (3%). Since there is no previous study on the endophytic fungi of Ziziphus plants, the whole fungi isolated in the present investigation are new records to these plants, whereas 45 species were reported for the first time in the mycoflora of Oman and 27 species are new to the mycoflora of Arabian Peninsula (Table 2).

EL-NAGERABI et al. – Endophytic fungi associated with Ziziphus Table 2. Number of cases of isolation (NCI, out of 18 samples), occurrence remarks (OR) and incidence percentage (I%) of endophytic fungi of Ziziphus spina-christi and Z. hajanensis Isolates

Record Z. spinachristi type NCI OR ®* 18 H ® 13 H ®Ψ 7 M ®Ψ 5 L ®Ψ 16 H ®Ψ 18 H ®Ψ 14 H ® 16 H ®Ψ 11 H ®Ψ 4 L ®Ψ 3 L ® 1 R ® 7 M ®Ψ 5 L ®* 14 H ®* 16 H ®* 18 H ®Ψ 8 M ® 6 L ® ®Ψ 2 R

Z. hajanensis NCI OR 7 M 6 M 4 L 11 H 9 M 12 H 5 L 2 R 8 M 4 L 10 H 2 R 2 R 3 L 1 R

Alternaria alternata 69 Alternaria chlamydospora 53 Alternaria cheiranthi 19 Alternaria cineraniae 14 Alternaria citri 56 Alternaria pluriseptata 81 Alternaria radicina 64 Alternaria tenuissima 78 Alternaria triticina 31 Alysidium resinae 11 Anguillospora longissima 8 Arthrinium sp. 3 Aspergillus spp. 33 Aspergillus caespitosus 19 Aspergillus flavus 61 Aspergillus fumigatus 56 Aspergillus niger 78 Aspergillus unguis 22 Aspergillus wentii 19 Bactrodesmium rahmii 8 Catenularia state of 8 Chaetosphaeria innumera Cladosporium spp. ® 8 M 3 L 31 Cladosporium chlorocephalum ® Ψ 5 L 14 Cladosporium cucumerinum ® 6 M 19 Cladosporium sphaerospermum ® 3 L 11 Cladosporium tenuissimum ® 12 H 8 M 56 Curvularia harveyi ®Ψ 3 L 8 Curvularia intermedia ®Ψ 5 L 2 R 19 Curvularia lunata ®* 10 H 8 M 50 Dendryphiella infuscans ®Ψ 2 R 6 Dissophora sp. ®Ψ 1 R 3 Drechslera australiensis ® 10 H 6 M 44 Drechslera biseptata ®Ψ 5 L 3 L 22 Drechslera hawaiiensis ® 9 M 7 M 44 Drechslera indica ®Ψ 6 M 4 L 28 Drechslera ravenelii ®Ψ 4 L 11 Drechslera spicifera ®* 11 H 8 M 53 Drechslera cactivora ®Ψ 5 L 14 Fusarium spp. ® 5 L 3 L 22 Fusarium chlamydosporum ® 7 M 5 L 33 Fusarium lateritium ® 3 L 8 Fusarium merismoides ®Ψ 2 R 66 Fusarium nivale ® 6 M 17 Fusarium reticulatum ® 3 L 8 Fusarium sambucinum ® 4 L 1 R 14 Hansfordia biophila ®Ψ 2 R 6 Hansfordia pulvinata ®Ψ 1 R 3 Helminthosporium sorghi ®Ψ 2 R 7 Penicillium spp. ® 6 M 2 R 22 Penicillium chrysogenum ® 2 R 6 Penicillium purpurogenum ® 3 L 1 R 11 Penicillium citrinum. ® 5 L 3 L 22 Phoma sorghina ® 1 R 3 Rhizopus stolonifer ®* 15 H 13 H 78 Trichocladium canadense ®Ψ 4 L 11 Trichodochium disseminatum ® Ψ 2 R 6 Ulocladium alternariae ®Ψ 7 M 4 L 31 Ulocladium consortiale ® 4 L 1 R 14 Yeasts * 12 H 5 L 47 Sterile mycelia ® 18 H 11 H 69 Note: *: Known to mycoflora of Oman; Ψ: New record to Arabian Peninsula; ® New record to the Ziziphus spp.; OR: Occurrence remarks, out of 18 samples; H: High, more than 9 samples; M: Moderate, between 6-9 samples; L: Low, between 3-5 samples; R: Rare, less than 3 samples;

The surface of plant tissues, especially leaves, are excellent reservoirs of several types of microorganisms including numerous endophytic fungi (Petrini 1991; Bokhary et al. 2000). Therefore, many fungal species were continuously isolated from the tissues of the most parts of terrestrial and aquatic plants (Devarajan et al. 2002; Huang et al. 2008). These fungi represent an important and quantifiable component of fungal biodiversity and are known to affect the biodiversity and structures of plant communities (Krings et al. 2007; Huang et al. 2008). Several studies of endophytic fungi from tropical and temperate forests support the high estimate of species diversity (Kumar and Hyde 2004; Santamaria and Bayman 2005; Santamaria and Diez 2005; Sänchez Märquez et al. 2007). Almost all the terrestrial plants studied have mitosporic, ascomycetes fungi and sterile forms as endophytes (Bill 1996; Devarajan et al. 2002). The present study showed that pigmented dematiaceous hyphomycetes (mitosporic fungi) and ascomycetes colonized the tissues of these plant species (Table 2). Some of these fungi such as the species of Alternaria alternata, A. angustiovoide, A. brassicicola, Cladosporium, Helminthosporium, Chaetomium, Drechslera, Aspergillus, Fusarium, Penicillium, Phoma, Ulocladium, and Camarosporium were isolated in similar study of halophytic Suaeda spp. and medicinal plants from China (Huang et al. 2008; Sun et al. 2011). The dark mycelia of these fungi benefit their host through absorption of more UV radiation compared to white mycelia (Sun et al. 2011). Therefore, these fungi might enhance the growth and improve ecological adaptation of the host plants by enhancing plant tolerance to environmental stresses and resistance to phytopathogens and/or herbivores as suggested by many authors (Clay and Schardl 2002; Waller et al. 2005; Barrow et al. 2007; Liu et al. 2010; Sun et al. 2011). Thus, it was suggested that the dark pigmented mycelia increase the host resistance to microbes and hydrolytic enzymes (Carlos et al. 2008; Sun et al. 2011). Normally various fungal taxa were isolated as endophytes from the leaf tissues of single plant species of tropical plants (Petrini 1991). Some of these fungi are pathogenic or saprophytic which under favorable conditions may become pathogenic; while there are others which live on the leaves only as saprophytes and get their nutrition from exudates of the leaves’ tissues, insect excretion or from air-borne organic matters deposited on the surface of the leaves (Last and Deighton 1965; Bokhary et al. 2000). The variations of foliar endophytes are due in part to genetic differences among trees and the variations in the environmental conditions (Elamo et al. 1999). In the investigation of species composition in woody plants, although large number of endophytes was obtained, few species dominated the community (Petrini et al. 1992). Some species of Alternaria, Colletotrichum and Fusarium have been reported as endophytes for many plants (liu et al. 2010). Phoma, Cladosporium, and Fusarium are frequently reported to occur as endophytes in terrestrial plants of the tropics (Brown et al. 1998). Alternaria spp., Cladosporium spp., Stemphylium spp., and Pleospora sp. were dominant endophytes of Salicornia europaea in Japan (Sun et al.

B I O D I V E R S IT A S 14 (1): 10-16, April 2013

2011). Alternaria alternata, Cladosporium cladosporioides and Penicillium chrysogenum are the most common endophytes isolated from halophytes of the Red Sea Coast of Egypt (El-Morsy 2000). Aspergillus niger was the dominant endophytic fungus in mangrove and legumes (Dorothy and Kandikere 2009). It is evident that dematiaceous fungi universally inhabit plants in different ecological zones and play important ecological roles for the survival of the plants. Generally many species of the genus Aspergillus such as A. fumigatus, and A. niger in addition to species of Penicillium and Fusarium are adapted to different plant tissues (Ilyas et al. 2009). In the present study, some of endophytic fungi isolated in similar studies (Petrini et al. 1992; Dorothy and Kandikere 2009; Ilyas et al. 2009; Sun et al. 2011) were recovered from the green leaves of the two species of Ziziphus plants whereas the remaining species were reported for the first time as endophytic fungi on these plant species (Table 2). These indicate the endophytic nature of fungi frequently isolated from the green leaves of these two Ziziphus species. Biodiversity of sterile mycelia Sterile mycelia consist of various morphological fungal types without any true spores. These fungi are considerably prevalent in endophytic investigations (Lacap et al. 2003; Huang et al. 2008). Of the frequently encountered endophytic fungal groups, sterile mycelia had the highest relative frequency (27.2%) (Huang et al. 2008). In the present study, 29 sterile mycelia were isolated from the tested samples with the highest occurrence remark and level of incidence (69%) (Table 2). These mycelia revealed different macroscopic and microscopic features and do not form reproductive structures when incubated for long period of time in order to enhance fungal sporulation. This suggests the high possibility of isolating more fungal species using advanced identification methods. Endophytic fungal community among different plant species Many plants are colonized by a characteristic population of microorganisms (Bowerman and Goos 1991). Endophytic fungi frequently demonstrate single host specificity at the plant species level, but this specificity could be influenced by seasonal changes of the climatic factors (Cohen 2004; Hung et al. 2008; Sun et al. 2011). Partial heterogeneity or geographic separations were used to indicate the endophytic fungal segregation impacted by environmental differences (Yahr et al. 2006). A recent study showed that endophytes are not host specific (Jalgaonwala et al. 2011). They colonize multiple host species of the same plant family within the same habitat, and their distribution can be similar in closely related plant species (Huang et al. 2008). A single endophyte or different strains of the same fungus can be isolated from different parts or tissues of the same host, which indicate their ability to utilize different substrates (Jalgaonwala et al. 2011). These variations in endophyte colonization could be caused by the difference in substrates and nutrients of the host tissues (Rodrigues 1994; Rodriguez et al. 2009). The most frequent endophytic fungal taxa from 29 medicinal plants had a nearly

ubiquitous presence in leaves and the stem of these plants (Huang et al. 2008). This may be attributed to differences in the structural and nutritional composition of the plant tissues (Rodrigues 1994; Rodriguez et al. 2009; Sun et al. 2011). In the present study (Table 2), the green leaves of Z. spina-christi and Z. hajanensis were similarly colonized by 31 species of endophytic fungi of variable levels of occurrence, whereas 19 species were specific to Z. spinachristi and 7 species were isolated from Z. hajanensis. The incidence levels of these fungi are evidently higher in the green leaves of Z. spina-christi comparable to Z. hajanensis. These indicate the possibility of some degree of species-specificity to these fungi as suggested by many authors (Cohen 2004; Hung et al. 2008; Sun et al. 2011) and with similar recovery at different incidence levels of endophytic fungi in these closely related Ziziphus species (Huang et al. 2008; Jalgaonwala et al. 2011). Seasonal biodiversity of endophytic fungi Little is known about the temporal changes in the endophytic fungal community. The diversity of endophytic fungi recovered from the selected plant is similar during summer (March-July) and winter (September-January). Almost the same species of fungi were isolated from the tissues of the plant, and there are no evident variations of fungal flora with the seasons. These results showed that fungal species colonizing the tissues of the plant were consistent during the growing seasons. This is may be due to the continuous growth of the mycelia within the tissues and production of new spores to invade new tissues (Sun et al. 2011). However, the abundance of endophytes varied among sampling times and did not increase over time. On the other hand, precipitation may influence the incidence of endophytes (Sahashi et al. 2000; Gรถre and Bucak 2007). More fungal endophytes developed in plant tissues in spring than in autumn and the higher rainfall in spring may enhance evidence dispersal of the fungal spores (Gรถre and Bucak 2007). It has been suggested that the smaller and the more scattered the plant fragments sampled, the higher the probability of approaching real diversity values of endophytic fungal communities (Gamboa and Bayman 2006). Fungal endophytes that colonize healthy plant tissues either remain dormant or produce more extensive but symptomless infections (Devarajan et al. 2002). In the present study, there are no apparent seasonal variations among of endophytic fungi associated with the two selected species of the genus Ziziphus as concluded in similar studies (Sun et al. 2011).

CONCLUSION We isolated 52 species of 21 genera of fungi, and 29 sterile mycelia and 17 yeasts from the green leaves of Z. spina-christi, Z. hajanensis. Some of these fungi are new records for the plants and/or to the mycoflora of Oman and Arabian Peninsula. There is no seasonal variation in the endophytic fungi; however, there is some degree of species-preference observed in the endophytic distribution as shown by the composition of the fungal community,

EL-NAGERABI et al. â&#x20AC;&#x201C; Endophytic fungi associated with Ziziphus

isolation frequencies and occurrence remarks. This study was conducted using classical taxonomic methods and identification techniques which do not facilitate the isolation of many fungi and identification of numerous yeasts and sterile mycelia. Therefore, our future studies should focus and utilize many molecular techniques which improve our research and knowledge of the biodiversity of the endophytic fungi.

ACKNOWLEDGEMENTS We thank the Department of Biological Sciences and Chemistry, College of Arts and Sciences, University of Nizwa, and Department of Biology, College of Science, Sultan Qaboos University for providing space and facilities to carry this research. We thank the University of Nizwa Writing Center for proof reading the English of this manuscript.

REFERENCES AlBahry SN, Elshafie AE, Deadman M. 2005. First report of Ganoderma colossum on Ficus altissima and Delonix regia in Oman. Pl Pathol 54: 245. AlKhanjari SS. 2005. Exploration and estimation of morphological and Genetic Diversity of wheat (Triticum spp.) landraces in Oman. Kassel University Press, GmbH, Kassel. Anon. 2008. Mountains of the world, ecology, conservation and sustainable development. Conservation of the environment, Diwan of the R. Court, Muscat, Sultan Qaboos University Press, Sultanate of Oman. Arnold AE. 2007. Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungi Biol Rev 21: 51-66. Barac T, Tghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Leile D. 2004. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22: 583-588. Barnett HL. 1955. Illustrated genera of imperfect fungi. Burgess Publishing Company, Minneapolis. Barnett HL, Hunter BB. 1998. Illustrated genera of imperfect Fungi. Prentice-Hall, Inc., New York. Barnett HL, Hunter BB. 2003. Illustrated genera of imperfect fungi. Burgess Publishing Company, Minneapolis.. Barrow J, Lucero M, Reyes-Vera I, Havstad K. 2007. Endosymbiotic fungi structurally integrated with leaves reveals a lichenous condition of C4 grasses. In Vitro Cell Dev Biol Pl 43: 65-70. Bhansali AK. 1975. Monographic study of the family Rhamnaceae of India. [Dissertation]. University of Jodhpur, India. [India] Bills GF. 1996. Isolation and analysis of endophytic fungi communities from woody plants. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants: Systematics, ecology and evolution. APS Press, Minnesota. Bokhary HA, AI-Sohaibany S, AI-Sadoon QH, Parvez S. 2000. Fungi associated with Calotropis procera and Capparis spinosa leaves. J King Saud Univ 12: 11-23. Borgi W, Chouchane N. 2009. Anti-spasmodic effects of Ziziphus lotus (L.) Desf. extracts on isolated rat duodenum. J Ethnopharmacol 126: 571-573. Borgi W, Recio MC, Rios JL, Chouchane N. 2008. Anti-inflammatory and analgesic activities of flavonoid and saponin fractions from Ziziphus lotus (L.) Lam. South African J Bot 74: 320-324. Bowerman L, Goos RD. 1991. Fungi associated with living leaves of Nymphaea odorata. Mycologia 83: 513-516. Brown KB, Hyde KD, Guest DI. 1998. Preliminary studies on endophytic fungal communities of Musa acuminata species complex in Hong Kong and Australia. Fugal Div 1: 27-51. Carlile MJ, Watkinson CS, Gooday GW. 2001. The fungi. Academic Press, London.

Carlos PT, Marcelo BS, Joshua DN, Luiz RT. 2008. Melanin as a virulence factor of Paracoccidioides brasiliensis and other dimorphic pathogenic fungi, a minireview. Mycopathologia 165: 331-339. Clay K, Schardl C. 2002. Evolutionary origins of ecological consequences of endophyte symbiosis with grasses. Amer Nat 160: s99-s127. Cohen SD. 2004. Endophytic-host selectivity of Discula umbrinella on Quercus alba and Quercus rubra characterized by infection, pathogenicity and mycelial compatibility. European J Pl Pathol 110: 713-721. Devarajan PT, Suryanarayanan TS, Geetha V. 2002. Endophytic fungi associated with the tropical seagrass Halophila ovalis (Hydrocharitaceae). Indian J Mar Sci 3: 73-74. Dorothy DA, Kandikere RS. 2009. Assemblage and diversity of fungal associated with mangrove wild legume Canavalia cathartica. Trop Subtrop Agroecosyst 10: 225-235. Elamo P, Helander MH, Saloniemi I, Neuvonen S. 1999. Birch family and environmental conditions affect endophytic fungi in leaves. Oecologia 118: 151-156. Ellis MB. 1971. Dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew. Ellis MB. 1976. More dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew. El-Morsy EM. 2000. Fungi isolated from the endorhizosphere of halophytic plants from Red Sea Coast of Egypt. Fungal Div 5: 43-54. Elshafie AE. 2005. Coprophilous mycobiota of Oman (summary). Mycotaxon 93: 355-357. Elshafie AE, Al-Bahry SN, Ba-Omar T. 2003. Nematophagous fungi isolated from soil in Oman. Sydowia 55: 18-32. Elshafie AE, Al-Lawatia T, Al-Bahry SN. 1999. Fungi associated with black tea and tea quality in the Sultanate of Oman. Mycopathologia 14: 89-93. Elshafie AE, Al-Mueine R, Al-Bahry SN, AlKindi AY. 2005. Nematophagous and non-nematophagous fungi belonging to the genera Arthrobotrys and Dactylella from soils in Oman. Kuwait J Sci Eng 32: 57-72. Elshafie AE, Al-Rashdi TA, Al-Bahry SN, Bakheit CS. 2002. Fungi and aflatoxins associated with spices in the Sultanate of Oman. Mycopathologia 155: 155-160. Elshafie AE, A-Shally NS. 1998. Mycoflora and mycotoxigenic moulds of pistachio nuts for human consumption in the Sultanate of Oman. Sci Technol 3: 1-6. Elshafie AE, Ba-Omar T. 2001. First report of Albizia lebbck dieback caused by Scytalidium dimidiatum in Oman. Mycopathologia 154: 3740. Farr DF, Bills GF, Chamuris GP, Rossmans AY. 1989. Fungi on pants and plant products in the United States. APS press, the American Phytopathological Society, St. Paul, Minnesota, USA. Gamboa M, Bayman P. 2006. Communities in endophytic fungi in leaves of a tropical timber tree (Guarea Guidonia: Meliaceae). Biotropica 33: 352-350. Gazis R, Chaverri P. 2010. Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3: 240-254. Gene J, Elshafie AE, Guarro J. 1993. Two new coprophilous Pezizales from the Sultanate of Oman. Mycotaxon 46: 275-284. GĂśre ME, Bucak C. 2007. Geographical and seasonal influence on the distribution of fungal endophytes in Laurus nobilis. Forest Pathol 37: 281-288. Huang WY, Cai YZ, Hyde KD, Corke H, Sun M. 2008. Biodiversity of endophytic fungi associated with 29 traditional Chinese medicinal plants. Fungal Div 33: 61-75. Ilyas M, Kanti A, Jamal Y, Hertina, Agusta A. 2009. Biodiversity of endophytic fungi associated with Uncaria gambier Roxb. (Rubiaceae) from west Sumatra. Biodiversitas 10: 23-28. Jalgaonwala RE, Mohite BVM, Mahajan RT. 2011. A review: natural products from plant associated endophytic fungi. J Microbiol Biotechnol 1: 21-32. Kobayashi T. 1970. Taxonomic studies of Japanese Diaphotthaceae with special reference to their life-histories. [Dissertation]. Hokkaido University, Hokkaido, Japan. [Japan] Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen FJ. 2007. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174: 648-657. Kumar DSS, Hyde KD. 2004. Biodiversity and tissue-recurrence of endophytic fungi from Tripterygium wilfordii. Fungal Div 17: 69-90.

B I O D I V E R S IT A S 14 (1): 10-16, April 2013

Lacap DC, Hyde KD, Liew ECY. 2003. An evaluation of the fungal morphotype concept based on rhibosomal DNA sequences. Fungal Div 12: 53-66. Last FT, Deighton FC. 1965. The non-parasitic mycoflora on the surface of living leaves. Trans Br Mycol Soc 48: 83-89. Liu C, Liu T, Yuan F, Gu Y. 2010. Isolating endophytic fungi from evergreen plants and determining their antifungal activities. Africa J Microbiol Res 4: 2243-2248. Maraghni M, Gorai M, Neffati M. 2010. Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Ziziphus lotus. South African J Bot 76: 453-459. Mathur N, Vyas A. 1995. Changes in lysozyme patterns of peroxidase and polyphenol oxidase by VAM fungi in roots of Ziziphus species. J Pl Physiol 145: 498-500. Mmbaga MT, Sauve RJ. 2009. Epiphytic microbial communities on foliage of fungicide treated and non-treated flowering dogwoods. Biol Control 49: 97-104. Nelson PE, Toussoun TA, Marasas WFO. 1983. Fusarium species. An illustrated manual for identification. The Pennsylvania State University Press, University Park and London, London. Petrini O. 1991. Fungal endophytes of tree leaves. In: Andrews JA, Hirano SS (eds). Microbial lcology of leaves, Springer, New York. Petrini O, Sieber TN, Toti L, Viret O. 1992. Ecology, metabolites production and substrate utilization in endophytic fungi. Nat Toxins 1: 185-196. Pietra F. 1997. Secondary metabolites from marine microorganisms: Bacterai, protozoa, algae and fungi. Achievements and prospects. Nat Prod Rep 14: 453-464. Pitt JI. 1979. The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic Press, New York. Raper KB, Fennell DI. 1965. The genus Aspergillus. Williams and Wilkins, Baltimore.

Rodrigues KF. 1994. The foliar endophytes of the Amazonian palm Euterpe oleracea. Mycologia 86: 376-385. Rodriguez RJ, White JF, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytol 182: 314-330. Sahashi N, Miyasawa Y, Kubono T, Ito S. 2000. Colonization of beech leaves by two endophytic fungi in northern Japan. Forest Pathol 30: 77-86. Samson RA, Hoekstra ES, Frisval JC, Filtenborg O. 1995. Introduction to Food-Borne Fungi. Holland Centraalbureau voor Schimmelcultures, Baarn. Sänchez Märquez S, Bill GF, Zabalgogeazcoa I. 2007. The endophytic mycobiota of the grass Dactylis glomerata. Fungal Div 27: 171-195. Santamaria J, Bayman P. 2005. Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microb Ecol 50: 1-8. Santamaria O, Diez JJ. 2005. Fungi in leaves, twigs and stem bark of Populus tremula from northern Spain. Forest Pathol 35: 95-104. Strobel GA. 2002. Rainforest endophytes and bioactive products. Critical Rev Biotechnol 22: 315-333. Sun Y, Wang Q, Lu XD, Okane I, Kakishika M. 2011. Endophytic fungi associated with two Suaeda species growing in alkaline soil in China. Mycosphere 2 (3): 239-248. Sutton BC. 1980. The coelomycetes. London, England, Commonwealth Mycological Institute, Kew. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hűchelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Nat Acad Sci USA 102: 13386-13391. Webster J. 1980. Introduction to fungi. Cambridge University Press, Melbourne. Yahr R, Vilgalys R, DePriest PT. 2006. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of lichen symbiosis. New Phytol 171: 847-860.

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 17-24

ISSN: 1412-033X E-ISSN: 2085-4722 DOI: 10.13057/biodiv/d140103

Dynamics of fish diversity across an environmental gradient in the Seribu Islands reefs off Jakarta HAWIS H. MADDUPPA1,♥, BEGINER SUBHAN1, ENY SUPARYANI2, ACHIS M. SIREGAR1, DONDY ARAFAT1, SUKMARAHARJA A. TARIGAN1, ALIMUDDIN1, DENNY KHAIRUDI1, FADHILLAH RAHMAWATI1, ADITYA BRAMANDITO1 1

Laboratory of Marine Biodiversity and Biosystematics, Department of Marine Science and Technology Faculty of Fisheries and Marine Science Bogor Agricultural University. Jl. Agatis No. 1, Bogor 16680, West Java, Indonesia. Tel./Fax. +62 251 8623644, e-mail: hawis@ipb.ac.id. 2 Office of Marine and Agriculture, Jakarta Province. Jl Gunung Sahari No XI, Jakarta Pusat 10720, Jakarta, Indonesia Manuscript received: 19 March 2013. Revision accepted: 17 April 2013.

ABSTRACT Madduppa HH, Subhan B, Suparyani E, Siregar AM, Arafat D, Tarigan SA, Alimuddin, Khairudi D, Rahmawati F, Bramandito A. 2013. Dynamics of fish diversity across an environmental gradient in the Seribu Islands reefs off Jakarta. Biodiversitas 14: 17-24. The reefs of Seribu Islands have been affected by multitude of anthropogenic pressures. However, the biodiversity of reef fishes across the archipelago linked to environmental condition is poorly known. This study aimed to investigate the biodiversity and the trophic level of fish communities across the archipelago. The study on reef fish communities was conducted on 33 reef sites associated with islands or shoal randomly chosen from each zone along environmental gradients from the inshore water nearest of Jakarta Bay to the offshore water of the outer islands. The study sites represented each sub-districts within the archipelago, namely Pari, Tidung, Panggang, Kelapa, and Harapan. A total of 46,263 individual fishes were counted, belonging to 216 species and 29 families. The multivariate analysis of fish abundance using the Bray Curtis similarity index and non-metric multidimensional scaling (MDS) clearly showed the clustering of sub-districts, near and far from Jakarta Bay. The results showed that the sub-districts can be clustered into three groups. Group one consists of one sub-district (Pari) located in the southern part of the Seribu Islands near Jakarta Bay. Group two consists of three subdistricts (Tidung, Panggang, Kelapa) located in mid of the archipelago. The third group consists of one sub-district (Harapan) located in the northern part of the Seribu Islands. Based on species richness and fish diversity indices, the sub-districts can be clustered into two groups (1 = Pari and Tidung, 2 = Panggang Kelapa, Harapan). However, levels of similarities among sub-districts varied. The fish community in sub-district of Pari was dominated by carnivorous, omnivorous and herbivorous fishes, while those in the rest of subdistricts were dominated by omnivorous and carnivorous fishes. The present study results showed that the biodiversity of reef fishes across the Seribu Islands seemed to be linked to the environmental conditions. Key words: Fish-habitat association, species diversity, anthropogenic stress, multivariate analysis

INTRODUCTION Coral reefs are heavily influenced by the human activities through pollution and habitat loss throughout the world (Burke et al. 2011), and sea level rise or the increase of ocean temperature due to the global change (Hughes et al. 2003). In Indonesia, marine communities have been impacted by an increase in eutrophication and sedimentation levels as shown in the waters of Jakarta Bay (Verstappen 1988; Marques et al. 1997; Renema 2008). As a result of increased sedimentation, nutrient loading, and chemical contamination, coral reefs became degraded (Rees et al. 1999; Williams et al. 2000). Furthermore, reef degradation could affect the coral reef fish communities due to their strong relationship. The Seribu Islands (or Thousand Islands, Kepulauan Seribu), which consists of 110 islands spread from the Jakarta Bay to as far as 80 km to the north of the Java Sea, have been threatened by different kinds of anthropogenic pressures including coral mining, fishing, anchor damage, oil spills, resort construction and the discharge of industrial

and domestic effluents (Rees et al. 1999; Rachello-Dolmen and Cleary 2007; Willoughby 1986; Uneputty and Evans 1997). In the 1980s, the archipelago reefs also experienced bleaching phenomenon due to ENSO (El Niño Southern Oscillation) resulting in the death of mainly branching species of the genera of Acropora and Pocillopora (Brown and Suharsono 1990). Regions of the Seribu Islands are divided into three zones according to environmental gradient from the inshore water of Jakarta Bay to the offshore water of the outer islands (Hutomo and Adrim 1985). Since reef studies in 1920s, the reefs surrounding Onrust Island, located in Jakarta Bay, have been excluded from reef studies due to measurable anthropogenic influences (Zaneveld and Verstappen 1952). The environmental pressures on Jakarta Bay have increased until today and have been noted in several studies (e.g. Tomascik et al. 1997). A number of studies also show that reef coverage in Jakarta Bay is very low and shifts toward the Seribu Islands, as a result of diminishing human activities and pollution (Verstappen 1988; Cleary et al. 2006).

B I O D I V E R S IT A S 14 (1): 17-24, April 2013

The gradient of environmental quality has changed the marine biodiversity across Seribu Islands, such as sponges (de Voogd and Cleary 2008), mollusk (van der Meij et al. 2009) and corals (Cleary et al. 2006). Complexity of coral reefs and spatial variability affect the trophic structure of the fish community. For instance, the decrease of live corals has increased the coverage of algae which in turn gives benefit to herbivorous fishes (Madduppa et al. 2012). Therefore, the current study aimed to investigate the biodiversity dynamics and the trophic levels of fish communities across the archipelago.

MATERIALS AND METHODS Study sites The Seribu Islands Marine National Park has been declared as a National Reserve in 1982 (Uneputty and Evans 1997). Since 2006, the Seribu Islands is administratively divided into two districts (Estradivari et al. 2007). First, The District of North Seribu Islands which covers 79 islands within three sub-districts i.e. Kelapa (36 islands), Harapan (30), and Panggang (13). Second, The District of South Seribu Islands which is divided into three sub-

Figure 1. Location of the Seribu Islands, north of Jakarta, Java Island, Indonesia. The map at the upper right shows the position of Seribu Islands relative to Indonesia. The sampling sites indicated by flag.

MADDUPPA et al. – Reef fish diversity linked to environmental gradient

A total of 46,263 individual fishes were counted, belonging to 216 species and 29 families (Table 1). A total of 49 and 78 fish species were recorded from sub-districts of Pari and Tidung, 109 and 148 from sub-districts of Panggang and Kelapa, and 106 from sub-district of Harapan. The values of species richness in this study were almost similar to that observed by Estradivari et al. (2007) in 2004-2005 in the Seribu Islands (211 species). In addition, the species richness of the Seribu Islands were also similar in range to those observed at other Indonesian coral reefs, such as Togean Islands and Weh Island (Allen and Werner 2002). The low species richness in the subdistricts of Seribu Islands near from Jakarta Bay (e.g. Pari and Tidung) might be related to the pressures on the environment such as bleaching resulting from the 1982/83 ENSO event (Brown and Suharsono 1990; Hoeksema 1991), and anthropogenic factors such as land-based contaminants, man-made objects, oil pollution, domestic and industrial refuse (Willoughby 1986; Uneputty and Evans 1997; Rees et al. 1999).

Acanthuridae Acanthurus sp. Ctenochaetus striatus Apogonidae Apogon angustatus Apogon apogonides Apogon aureus Apogon cavitienis Apogon chrysopomus Apogon compressus Apogon novemfasciatus Apogon sealei Apogon semiornatus

Harapan

Family Species

Kelapa

Table 1. Total number and trophic level of fish species at each subdistrict in the Seribu Islands Panggang

Data analysis The community Shannon-Wiener diversity index H’ was calculated on a natural logarithm (ln) basis (Magurran 1988; Shannon and Weaver 1949). Poisson regression analysis was used to test the statistical significance of differences in fish abundance among sites (sub districts), as

RESULTS AND DISCUSSION

Tidung

Data collection Sampling was carried out at each site between 09.00 and 16.30, November 10-20, 2011 during a coral reef expedition by Marine Biology Laboratory, Bogor Agricultural University. Reef fish communities were assessed by underwater visual census (UVC) on a transect line of 50 meters at each depth (English et al. 1997). In an attempt to reduce daily variability of fish density data (caused by differences in nocturnal and diurnal behavior), sampling excluded the high activity periods of early morning and late afternoon (Colton and Alevizon 1981; English et al. 1997). During each census, the observer waited for 5 to 10 minutes before beginning the data recording along transect in order to allow the fishes to resume their normal behaviours (Brock 1982; Halford and Thompson 1994). Only individuals within 2.5 m on either side and 5 m above along the transect, were counted. Each individual (cryptic and large pelagic species were excluded) was counted and identified to species level. In order to avoid the influence of temporal recruitment events, fish recruits up to a size of ~3-5 cm were excluded from the count. After data collection, reef fish identification was confirmed by using standard fish identification books (i.e. Allen 2000; Kuiter 1992). The trophic level for each species was confirmed with the Fishbase (Froese and Pauly 2010).

well diversity and species richness, using statistical package STATISTICA 7.0. Multivariate analysis of the fish community data were conducted using the program PRIMER 5.2.9 (Clarke and Gorley 2001; Kruskal 1964). Fish abundance, species richness, and species diversity data were fourth-root transformed prior to analysis to reduce the influence of some overlay abundant species and give more weight to rare species while retaining the information value of relative abundances, an approach frequently used in the multivariate analysis of community data (Clarke and Green 1988; Field et al. 1982). Bray-Curtis similarity and Non-metric Multidimensional Scaling (MDS) were performed to visualize differences in fish communities from the different sites (Kruskal 1964; Shepard 1962). MDS was based on Bray-Curtis similarities, and 100 restarts were used for the calculations.

Herbivore 0 Omnivore 0

1 1

1 0

0 4

0 0

Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore

0 0 0 0 13 20 0 0 0

0 80 11 20 0 331 24 0 17

7 23 37 0 0 293 0 0 0

0 0 89 0 0 192 43 0 2

Trophic

Pari

districts covering 31 islands. The Seribu Islands Marine National Park which covers an area of 107.489 ha or approximately 20% of the total region. Two different seasons are affecting the Seribu Islands, namely ‘wet’ season (November-March) during the northwest monsoon, and ‘dry’ season (May-September) during the southeast monsoon (Rees et al. 1999). Figure 1 shows the study sites at Seribu Islands. The study on reef fish communities was conducted at 33 reef sites associated with islands or shoal which were randomly chosen from each zone along environmental gradients from the inshore water nearest of Jakarta Bay to the offshore water of the outer islands and represented each sub-districts within the archipelago, namely Pari (Lancang Is., Bokor Is.), Tidung (Tidung Besar Is., Payung Besar Is., Karang Beras), Panggang (Karang Bongkok, Gosong Air, Kotok Kecil Is., Karang Congkak, Sekati Is., Semak Daun Is., Air Barat Is., Kotok Besar Is.), Kelapa (Genteng Is., Jukung Is., Kaliage Besar Is., Kaliage Kecil Is., Kayu Angin Semut Is., Kelapa Is., Lipan Is., Malinjo Is., Matahari Is., Melintang Is., Satu Is., Semut Besar Is., Semut Timur Is.), and Harapan (Opak Besar Is., Opak Kecil Is., Sepa Besar Is., Sepa Kecil Is.). Two different depths (3 and 10 m) for each sampling site at reef slope were selected (English et al. 1997).

0 0 0 0 0 2 0 20 0

B I O D I V E R S IT A S 14 (1): 17-24, April 2013

20 Archamea fucata Cheilodipterus artus Cheilodipterus isostigmus Cheilodipterus sp. Sphaeramia nematoptera Aulostomidae Aulostomus chinensis Balistidae Balistoides sp. Melichthys indicus Caesionidae Caesio cuning Caesio teres Pterocaesio digramma Pterocaesio tile Centriscidae Aeoliscus strigatus Chaetodontidae Chaetodon collare Chaetodon meyeri Chaetodon octofasciatus Chelmon rostratus Chaetodon melanopus Coradion trifasciatus Heniochus chrysostomus Heniochus pleurotaenia Heniochus varius Cirrhitidae Paracirrhites sp. Dasyatidae Taeniura lymma Echeneidae Remora sp. Ephippidae Platax pinnatus Platax teira Gobiidae Exyrias belissimus Istigobius decorates Haemulidae Plectorhinchus chaetodontoides Plectorhinchus chrysotaenia Plectorhinchus vittatus Hemirhamphidae Hemirhamphus far Holocentridae Myripristis berndti Myripristis sp. Sargocentron diadema Sargocentron rubrum Sargocentron sp. Sargocentron tiereoides Labridae Anampses sp. Bodianus mesothorax Cheilinus chlorourus Cheilinus diagramma Cheilinus fasciatus Cheilinus hortulanus Cheilinus oxyrhynchus Cheilinus trilobatus Cheilinus unifasciatus Choerodon anchorago Choerodon fasciatus Cirrhilabrus cyanopleura Ctenochaetus striatus Diproctacanthus xanthurus Epibulus insidiator Gomphosus varius Halichoeres binotopsis Halichoeres biocellatus Halichoeres chloropterus Halichoeres chrysotaenia Halichoeres dussumieri Halichoeres hortulanus

Carnivore Carnivore Carnivore Carnivore Carnivore

0 0 2 0 0

0 0 0 0 0

3 52 0 0 0

0 33 0 24 22

0 88 0 0 0

Carnivore 0

Carnivore 0 Omnivore 0

1 0

0 7

0 0

0 2

Planktivore 0 Planktivore 0 Carnivore 0 Planktivore 0

0 260 0 0

429 372 0 38

209 906 0 80

116 475 50 0

Carnivore 4

Herbivore Herbiivore Coralivore Coralivore Coralivore Coralivore Coralivore Coralivore Coralivore

0 0 57 0 0 0 1 3 0

0 5 131 3 0 3 0 2 11

0 5 196 9 0 0 0 0 7

0 0 66 2 2 6 0 4 1

Carnivore 1

Carnivore 0

Omnivore 2

Omnivore 0 Omnivore 1

0 2

2 2

0 3

0 0

Omnivore 0 Omnivore 0

0 0

0 7

1 8

0 1

Carnivore 0 Carnivore 0 Carnivore 0

0 0 0

0 8 0

2 0 2

0 0 0

Omnivore 0

Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore

1 0 0 2 0 0

0 0 20 0 0 11

0 5 0 0 19 0

0 0 0 0 0 0

0 19 0 0 67 15 0 0 0 2 4 1930 7 2 0 0 0 18 45 7 21 29

1 0 27 24 7 0 15 0 96 19 8 0 6 0 3 0 6 0 32 0 25 23 3782 1770 0 0 27 52 6 0 9 0 2 1 39 19 30 0 21 0 0 53 80 20

1 0 0 0 0 0 0 0 0

0 0 0 0 0 0

Carnivore 0 0 Carnivore 1 6 Carnivore 0 0 Carnivore 0 0 Carnivore 0 29 Carnivore 0 0 Carnivore 0 0 Carnivore 0 0 Carnivore 0 0 Carnivore 1 10 Carnivore 0 0 Planktivore 400 1402 Omnivore 0 0 Corallivore 1 16 Carnivore 0 1 Carnivore 0 0 Carnivore 0 5 Carnivore 0 0 Carnivore 0 0 Carnivore 0 5 Omnivore 0 0 Carnivore 3 17

Halichoeres leucurus Halichoeres marginatus Halichoeres melanochir Halichoeres melanurus Halichoeres nigrescens Halichoeres ornatissimus Halichoeres richmondi Halichoeres scapularis Halichoeres sp. Halichoeres vrolikii Hemigymnus melapterus Labroides chrysotaenia Labroides dimidiatus Macropharyngodon negrosensis Neoglyphidodon melas Pseudocheilinus hexataenia Pseudojuloides cerasinus Pteragogus amboinensis Stethojulis trilineata Thalassoma lunare Thalassoma lutescens Thalassoma purpureum Thalassoma quinquevittatum Lethrinidae Lethrinus erythropterus Lutjanidae Lutjanus biguttatus Lutjanus decussatus Lutjanus kasmira Lutjanus russellii Mullidae Parupeneus barberinus Muraenidae Gymnothorax javanicus Nemipteridae Pentapodus caninus Pentapodus sp. Pentapodus vitta Scolopsis bilineatus Scolopsis ciliatus Scolopsis lineatus Scolopsis margaritifer Scolopsis sp. Scolopsis temporalis Scolopsis trilineatus Pempheridae Pempheris oualensis Pempheris sp. Pomacanthidae Centropyge vrolikii Chaetodontoplus mesoleucus Pomacanthus sextriatus Pomacentridae Abudefduf bengalensis Abudefduf curacao Abudefduf septemfasciatus Abudefduf sexfasciatus Abudefduf sordidus Abudefduf vaigiensis Acanthochromis polyancanthus Amblyglyphidodon aureus Amblyglyphidodon batunai Amblyglyphidodon curacao Amblyglyphidodon leucogaster Amblyglyphidodon nigroris Amphiprion akallopisos Amphiprion akindinos Amphiprion clarkii Amphiprion ocellaris Amphiprion perideraion Amphiprion sandaricinos Cheiloprion labiatus Chlororus sordidus Chromis amboinensis Chromis atripectoralis

Omnivore Omnivore Omnivore Omnivore Carnivore Carnivore Carnivore Carnivore Omnivore Omnivore Carnivore Omnivore Carnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Carnivore Carnivore

4 0 0 3 14 0 0 1 6 5 3 0 6 0 0 0 0 0 0 24 0 0 0

13 4 0 11 2 0 9 0 8 0 4 0 16 0 0 0 0 0 11 78 2 0 0

45 15 28 67 2 12 28 0 74 0 10 0 44 2 0 5 18 0 0 132 0 11 16

58 41 48 47 1 30 22 0 8 1 26 0 61 7 0 7 0 0 0 195 0 7 0

39 22 5 29 0 0 11 0 1 0 4 2 27 8 0 11 18 22 3 45 5 22 19

Carnivore 0

Carnivore Carnivore Omnivore Carnivore

0 0 0 0

2 6 0 0

4 25 0 0

26 25 6 4

0 3 0 0

Carnivore 0

Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore

0 0 0 22 3 0 6 0 0 0

46 0 0 29 0 17 0 0 0 0

28 1 18 50 9 14 41 4 0 26

28 0 0 17 0 17 0 0 0 12

Carnivore 0 0 Carnivore 50 0

0 0

15 0

36 0

Herbivore 0 Herbivore 0 Herbivore 0

1 19 0

0 57 2

0 0 199 69 0 0

Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore

0 0 0 111 0 94 0 2 0 114 16 39 0 0 0 0 0 0 0 0 90 39

0 0 19 107 49 119 0 0 49 519 226 0 2 0 0 0 0 0 0 0 50 708

91 18 0 204 0 139 11 25 79 560 342 0 12 0 3 0 0 0 3 2 93 500

0 0 0 3 0 0 0 0 1 1

0 0 3 0 0 0 0 0 0 20 0 0 2 0 0 0 0 0 0 0 0 0

25 0 0 121 0 61 13 2 87 451 163 0 0 5 3 6 2 4 0 0 94 878

MADDUPPA et al. – Reef fish diversity linked to environmental gradient Chromis fumea Chromis nitida Chromis scotochilopterus Chromis smithi Chromis ternatensis Chromis viridis Chromis xanthura Chrysiptera cyanea Chrysiptera hemicyanea Chrysiptera parasema Chrysiptera sp. Dascyllus melanurus Dascyllus reticulatus Dascyllus trimaculatus Diproctacanthus xanthurus Dischistodus melanotus Dischistodus perspicillatus Dischistodus prosopotaenia Hemiglyphidodon plagiometopon Neoglyphidodon bonang Neoglyphidodon crossi Neoglyphidodon leucogaster Neoglyphidodon melas Neoglyphidodon nigroris Neoglyphidodon thoracotaeniatus Neopomacentrus anabatoides Neopomacentrus bankieri Neopomacentrus cyanomos Neopomacentrus filamentosus Pomacentrus alexanderae Pomacentrus amboinensis Pomacentrus brachialis Pomacentrus burroughi Pomacentrus coelestis Pomacentrus cuneatus Pomacentrus javanicus Pomacentrus lepidogenys Pomacentrus littoralis Pomacentrus milleri Pomacentrus moluccensis Pomacentrus simsiang Pomacentrus smithi Pomacentrus sp. Pomacentrus xanthosternus Premnas biaculatus Pristotis obtusirostris Scaridae Chlorurus bleekeri Chlorurus microrhinos Chlorurus sordidus Scarus chameleon Scarus dimidiatus Scarus flavipectoralis Scarus frenatus Scarus ghobban Scarus globiceps Scarus niger Scarus quoyi Scarus rivulatus Scarus sordidus Scarus sp. Scarus xanthopleura Scorpaenidae Pterois volitans Serranidae Cephalopholis argus Cephalopholis boenak Cephalopholis microprion Cephalopholis sp. Diploprion bifasciatum Epinephelus fasciatus Epinephelus merra Epinephelus rivulatus Epinephelus sexfasciatus

Planktivore 80 Omnivore 0 Planktivore 0 Omnivore 0 Planktivore 14 Omnivore 0 Planktivore 0 Omnivore 0 Omnivore 0 Planktivore 0 Omnivore 6 Omnivore 0 Omnivore 0 Omnivore 0 Corallivore 0 Herbivore 0 Herbivore 0 Herbivore 0 Herbivore 0 Omnivore 0 Omnivore 0 Carnivore 0 Omnivore 2 Omnivore 3 Omnivore 0 Planktivore 0 Carnivore 0 Carnivore 0 Planktivore 0 Omnivore 1 Omnivore 0 Omnivore 6 Herbivore 1 Omnivore 0 Omnivore 7 Omnivore 0 Planktivore 13 Omnivore 0 Omnivore 5 Omnivore 5 Omnivore 0 Omnivore 50 Omnivore 5 Omnivore 0 Omnivore 1 Omnivore 0

0 0 0 0 52 142 0 0 0 0 0 0 0 1 1 0 0 24 0 0 25 25 19 18 0 0 0 0 0 1338 0 0 22 0 0 14 33 18 14 306 0 657 1 12 0 0

0 0 24 0 2 159 69 10 21 30 0 0 0 0 0 47 0 64 3 2 167 0 27 37 0 0 0 0 120 2320 0 0 23 56 0 0 33 0 0 378 0 775 0 0 0 18

50 303 5 0 0 34 17 0 926 712 372 177 78 70 0 0 21 9 22 32 0 0 1 0 1 0 80 10 2 0 48 35 10 0 101 32 24 5 0 0 58 94 0 0 111 117 129 17 88 0 38 0 0 20 156 0 178 71 4058 1335 57 0 0 0 77 5 0 12 0 0 0 0 514 98 0 0 56 11 297 103 16 0 2760 239 9 2 0 0 2 0 0 23

Herbivore Herbivore Omnivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore Herbivore

0 0 9 0 0 0 0 0 2 7 8 42 0 26 0

1 8 33 0 6 6 5 2 5 27 8 17 0 0 0

18 29 107 0 0 0 0 17 7 37 8 35 5 11 5

0 0 39 4 21 18 10 1 18 5 0 13 0 1 0

Carnivore 0

Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore Carnivore

0 1 4 0 1 0 0 0 0

0 0 4 0 0 0 0 7 5

26 13 16 1 0 1 2 6 1

0 0 2 0 0 0 0 6 4

0 0 0 0 0 0 0 0 0 2 0 0 0 2 0

0 4 1 1 0 0 0 0 0

Siganidae Siganus argenteus Siganus canaliculatus Siganus guttatus Siganus virgatus Siganus vulpinus Zanclidae Zanclus cornotus

Herbivore Herbivore Herbivore Herbivore Herbivore

0 0 0 0 0

0 7 0 3 3

0 0 0 0 0

0 0 12 16 0

1 0 0 0 0

Herbivore 0

The composition of the five most diverse fish families that were observed in all sub-districts are given in Table 2. The most abundant families at sub district of Pari were Labridae (wrasses), followed by Pomacentridae (damselfishes). The most abundant families at the rest subdistricts were Pomacentridae (damselfishes), followed by the Labridae (wrasses). Overall, the most diverse families in the reef community were Pomacentridae and Labridae. This pattern was also observed in the previous study at the islands (Estradivari et al. 2007), and at other locations in Indonesia (Ferse 2008). Table 2 The composition of the 5 most diverse fish families (%)observed in all sub-districts Family

Pari Tidung Panggang Kelapa Harapan

Apogonidae Caesionidae Chaetodontidae Labridae Nemipteridae Pempheridae Pomacentridae Scaridae

3.0 59.8 0.6 6.3 28.4 -

4.8 1.1 30.5 59.6 1.7

5.0 7.8 1.4 24.7 57.6 -

2.2 6.0 23.9 62.2 1.4

4.5 6.4 24.8 59.7 1.4

The Shannon-Wiener diversity indices of the fish communities, the average species richness and the average fish abundance are shown in Figure 2. The sub-district Pari as the nearest to Jakarta Bay, had the lowest fish abundance, species richness, fish diversity, while the subdistrict Harapan as the outlier islands had the highest ones. The fish abundance ranged from 265 ± 140 (sub-district of Pari) to 1154 ± 208 ind/250m2 (sub-district of Harapan). Similar patterns were also found for the diversity indices (H’) which ranged between 1.8 ± 0.15 (Pari) and 2.5 ± 0.17 (Harapan), and for the species richness which ranged from 20 ± 7 (Pari) to 36 ± 5 species/250m2 (Harapan) over the entire study period. The pattern showed that values on the fish abundance, diversity index and species richness increase toward north of Seribu Islands. The high abundance and species richness might be related to live coral coverage. The nearest region to Jakarta Bay has lowest live coral coverage and the live coral coverage increase toward to the north of the islands (Estradivari et al. 2007). In the present study, the sub-district’s reefs did have a significant influence on fish abundance and species richness, but not for diversity index (Table 3). Multiple studies have reported a positive correlation with the structural complexity of a coral reef habitat for fish abundance (e.g. Walker et al. 2009), species richness (e.g. Wilson et al. 2007), and species diversity (e.g. Öhman and Rajasuriya 1998).

B I O D I V E R S IT A S 14 (1): 17-24, April 2013

Table 3 Results of Poisson regression for abundance, species richness, and diversity of fish assemblages (*<0.001, n.s. not significant) Variable

Factor df

Abundance Site Species richness Site Shannon-Wiener index (H') Site

4 4 4

W.S

1868.0 0.00 21.083 0.00 0.50872 0.97

* * n.s

by omnivorous and carnivorous fishes. Even though there is a strong correlation between coral and fish, only few of the species found in a coral reef ecosystem depend specifically on scleractinian corals (Munday et al. 2007). A study indicated that the fish communities were likely not structured by habitat-mediated factors such as predation impact or available space, but different factors such as recruitment or migration were playing a stronger role (Madduppa et al. 2012). However, no significant differences in diversity indices were found among the subdistricts (Table 3). This might be explained by feeding specialization among coral fishes. The specialization in food can reduce competition within a reef (Gladfelter and Johnson 1983; Ross 1986), and increase species diversity. A study found that some species such as scarids appeared in only specific habitat which had the lowest amount of live coral but the highest amount of dead coral and algae (Madduppa et al. 2012). Other species such as Chaetodonts have been observed to appear on high percentage of live coral which they use for food or shelter (Cox 1994).

Figure 3. Distribution and mean composition of reef fish per sub districts at Seribu Islands based on trophic categories

Sub-district of the Seribu Islands

Figure 2. The average values of (a) fish abundance, (b) species richness, and (c) species diversity (Shannon-Wiener Index; ln basis) of fish assemblages at the sampling sites. The arrow shows the direction from Jakarta Bay to the offshore water of the outer islands.

Besides being used as a territory (Waldner and Robertson 1980; Patton 1994), coral reefs are source of food for fishes (Reese 1981). The percentage of trophic level of total fish species at each sub-district is shown in Figure 3. The trophic level of species at each sub-district varied. The fish community in sub-district of Pari was dominated by carnivorous, omnivorous and herbivorous fishes, while those in the rest sub-districts were dominated

The multivariate analysis of fish abundance, species richness and fish diversity were done using the Bray Curtis similarity index and non-metric multidimensional scaling (MDS). The MDS plot and Bray-Curtis similarity have distinctly clustered the sub-districts from southern and toward north of the Seribu Islands based on fish abundance, species richness and fish diversity. The results showed that the sub-districts can be clustered into 3 groups based on fish abundance, with 0 stress value (Figure 4). Group one consists of one sub-district (Pari) located in the southern part of the Seribu Islands near Jakarta Bay. Group two consists of three sub-districts (Tidung, Panggang, and Kelapa) located in mid of the archipelago. The third group consists of one sub-district (Harapan) located in the northern part of the Seribu Islands. The species richness and fish diversity indices showed that the sub-districts can be clustered into two groups (1=Pari and Tidung, 2= Panggang Kelapa, Harapan). These figures showed that the islands within archipelago seemed to be linked to the environmental factors such sedimentation, pollution and other human activities in Jakarta Bay and Seribu Islands (Rees et al. 1999; Rachello-Dolmen and Cleary 2007; Willoughby 1986).

MADDUPPA et al. – Reef fish diversity linked to environmental gradient

Figure 4. Dendogram based on Bray-curtis similarity (left) and MDS plot (right) of fish communities at the Seribu Islands, showing pattern of association among 216 species based on abundance (a), species richness (b) and fish diversity (c)

CONCLUSION Altogether, in spite of low replicate of transects in each studied reefs, the present study results showed that the biodiversity of reef fishes across the Seribu Islands seems to be linked to environmental condition such as turbidity and level of pollution from Jakarta Bay toward the northern of the islands. Further studies of reef fish communities and habitat characteristics throughout the region are needed to document environmental changes over time.

ACKNOWLEDGEMENTS We wish to thank the following institutions and people for their assistance and help during this study. Marine Biological Laboratory, Bogor Agricultural University (IPB) Bogor for the logistic support, members of Fisheries Diving Club, Bogor Agricultural University (IPB) Bogor for all their help in the field work. The study was supported

by Agency of Fisheries and Marine Affairs, Government of DKI Jakarta.

REFERENCES Allen GR. 2000. Marine fishes of South-East Asia. Periplus Editions (HK) Ltd, Singapore. Allen GR, Werner TB. 2002. Coral Reef Fish Assessment in the ‘Coral Triangle’ of Southeastern Asia. Environ Biol Fish 65: 209-214. Brock RE. 1982. A critique of the visual census method for assessing coral reef fish populations. Bul Mar Sci 32: 269-276. Brown BE, Suharsono. 1990. Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia. Coral reefs 8: 163-170. Burke L, Reytar K, Spalding M, Perry A. 2011. Reefs at Risk Revisited. World Resources Institute (WRI), Washington DC. Clarke KR, Gorley NR. 2001. PRIMER v5: Unser manual/tutorial. PRIMER-E Ltd., Plymouth. Clarke KR, Green RH. 1988. Statistical design and analysis for a ‘biological effects’ study. Mar Ecol Prog Ser 46: 213-226.

B I O D I V E R S IT A S 14 (1): 17-24, April 2013

Cleary DFR, Suharsono, Hoeksema BW. 2006). Coral diversity across a disturbance gradient in the Pulau Seribu reef complex off Jakarta, Indonesia. Biodiversity and Conservation. 15: 3653-3674. Colton DE, Alevizon WS. 1981. Diurnal variability in a fish assemblage of a Bahamian coral reef. Environ Biol Fish 6: 341-345. Cox EF. 1994. Resource use by Corallivorous Butterflyfishes (Family Chaetodontidae) in Hawaii. Bull Mar Sci 54: 535-545. de Voogd NJ, Cleary DFR. 2008. An analysis of sponge diversity and distribution at three taxonomic levels in the Thousand Islands/Jakarta Bay reef complex,West-Java, Indonesia. Mar Ecol 29: 205-215 English S, Wilkinson C, Baker V. 1997. Survey manual for tropical marine resources. Australian Institute of Marine Science (AIMS), Townsville. Estradivari, Syahrir M, Susilo N, Yusri S, Timotius S. 2007. Coral Reef Jakarta: long-term observations of coral reefs Seribu Islands (20052007). Yayasan TERANGI, Jakarta. [Indonesian]. Ferse SCA. 2008. Artificial reef structures and coral transplantation: fish community responses and effects on coral recruitment in North Sulawesi/Indonesia. [Dissertation]. University of Bremen, Bremen, Germany. Field JG, Clarke KR, Warwick RM. 1982. A practical strategy for analysing multispecies distribution patterns. Mar Ecol Prog Ser 8: 3752. Froese R, Pauly D. 2010. FishBase. World Wide Web electronic publication. www.fishbase.org Gladfelter WB, Ogden JC, Gladfelter EH. 1980. Similarity and Diversity Among Coral Reef Fish Communities: A comparison between Tropical Western Atlantic (Virgin Islands) and Tropical Central Pacific (Marshall Islands) Patch Reefs. Ecology 61: 1156-1168. Halford AR, Thompson AA. 1994. Visual census surveys of reef fish. Long-term monitoring of the Great Barrier Reef. Australian Institute of Marine Science (AIMS), Townsville. Hoeksema BW. 1991. Control of bleaching in mushroom coral populations (Scleractinia: Fungiidae) in the Java Sea: stress tolerance and interference by life history strategy. Mar Ecol Prog Ser 74: 225237. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301: 929-933. Hutomo M, Adrim M. 1985. Distribution of reef fish along transects in Bay of Jakarta and Kepulauan Seribu. In: Human induced damaged to coral reefs. Unesco Reports in Mar. Sci. 40: 135-156. Kruskal JB. 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29: 1-27. Kuiter RH. 1992. Tropical reef-fishes of the Western Pacific, Indonesia and adajacent waters. Gramedia, Jakarta. Madduppa HH, Ferse SCA, Aktani U, Palm HW. 2012. Seasonal trends and fish-habitat associations around Pari Island, Indonesia: setting a baseline for environmental monitoring. Environ Biol Fish 95:383398. Magurran AE. 1988. Ecological diversity and its measurement. Princeton University Press, Princeton.

Marques JC, Pardal MÂ, Nielsen SN, Jørgensen SE. 1997. Analysis of the properties of energy and biodiversity along an estuarine gradient of eutrophication. Ecol Modell 102, 155-167. Munday PL, Jones GP, Sheaves M, Williams AJ, Goby G. 2007. Vulnerability of fishes on the Great Barrier Reef to climate change. In: Johnson J, Marshall P (eds) Climate change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority, Townsville. Öhman MC, Rajasuriya A. 1998. Relationships between habitat structure and fish communities on coral. Environ Biol Fish 53: 19-31. Patton WK. 1994. Distribution and ecology of animals associated with branching corals (Acropora spp.) from the Great Barrier Reef, Australia. Bul Mar Sci 55:193-211 Rachello-Dolmen PG, Cleary DFR. 2007. Relating coral traits to environmental conditions in the Jakarta Bay/Pulau Seribu reef complex, Indonesia. Estuar Coast Shelf Sci 73: 816-826. Reese JG, Setiapermana D, Sharp VA, Weeks JM, Williams TM. 1999. Evaluation of the impacts of land-based contaminants on the benthic faunas of Jakarta Bay, Indonesia. Oceanologica Acta 22: 627-640. Renema W. 2008. Habitat selective factors influencing the distribution of larger benthic foraminiferal assemblages over the Kepulauan Seribu. Mar Micropaleontol 68: 286-298. Ross ST. 1986. Resource partitioning in fish assemblages: a review of field studies. Copeia 1986:352-388 Shannon CE, Weaver W. 1949. The mathematical theory of communication. University of Illinois Press, Urbana. Shepard R. 1962. The analysis of proximities: multidimensional scaling with an unknown distance function. II. Psychometrika 27: 219-246. Tomascik T, Mah A J, Nontji A, Moosa MK. 1997. The Ecology of the Indonesian Seas, Part One and Two. Periplus, Hongkong. Uneputty PA, Evans SM. 1997. Accumulation of beach litter on Islands of the Kepulauan Seribu Archipelago, Indonesia. Mar Poll Bull 34 (8): 652-655. van der Meij SET, Moolenbeek RG, Hoeksema BW. 2009. Decline of the Jakarta Bay molluscan fauna linked to human impact. Mar Poll Bull 59: 101-107. Verstappen HTh. 1988. Old and new observations on coastal changes of Jakarta Bay: an example of trends in urban stress on coastal environments. J Coast Res 4 (4): 573-587. Waldner RE, Robertson DR. 1980. Patterns of habitat partitioning by eight species of territorial Caribbean damselfishes (Pisces: Pomacentridae). Bul Mar Sci 30:171-186 Walker BK, Jordan LKB, Spieler RE. 2009. Relationship of Reef Fish Assemblages and Topographic Complexity on Southeastern Florida Coral Reef Habitats. J Coast Res 39-48. Williams TM, Rees JG, Setiapermana D. 2000. Metals and trace organic compounds in sediments and waters of Jakarta Bay and the Pulau Seribu Complex, Indonesia. Mar Poll Bull 40 (3): 277-285. Willoughby NG. 1986. Man-made litter on the shores of the Thousand Island Archipelago, Java. Mar Poll Bull 17: 224-228. Wilson S, Graham N, Polunin N. 2007. Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar Biol 151: 1069-1076. Zaneveld JS, Verstappen HTH. 1952. A recent investigation about the geomorphology and the flora of some coral islands in the Bay of Djakarta. J Sci Res 3: 58-68.

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 25-30

ISSN: 1412-033X E-ISSN: 2085-4722 DOI: 10.13057/biodiv/d140104

Variability of soil physical indicators imposed by beech and hornbeam individual trees in a local scale YAHYA KOOCH1,â&#x2122;Ľ, SEYED MOHSEN HOSSEINI1, SEYED MOHAMMAD HOJJATI2, ASGHAR FALLAH2 1

Department of Forestry, Faculty of Natural Resources & Marine Sciences, Tarbiat Modares University, 46417-76489, Noor, Mazandaran, Iran. Tel: +98-122-6253101 (-3), Fax: +98-122-6253499, ď&#x201A;Šemail: yahya.kooch@modares.ac.ir 2 Department of Forestry, University of Natural Resources and Agriculture Sciences of Sari, Mazandaran, Iran. Manuscript received: 25 March 2013. Revision accepted: 26 April 2013.

ABSTRACT Kooch Y, SM Hosseini, Hojjati SM, Fallah A. 2013. Variability of soil physical indicators imposed by beech and hornbeam individual trees in a local scale. Biodiversitas 14: 25-30. The objective of our study was to determine if soil physical indicators could be related to the influence of the individual trees in stands of mixed species growing on steep slopes in the Hyrcanian forests of Iran. Research was conducted in a forest dominated by beech (Fagus orientalis Lipsky) and hornbeam (Carpinus betulus L.) interspread with the other deciduous tree species. Due to, twenty hectare areas of Experimental Forest Station of Tarbiat Modares University was considered in northern Iran. The positions of trees with diameter at breast height more than 45cm were recorded by Geographical Position System (GPS). Three single-trees (trees with canopy cover separated from other trees and covered distinguished space) considered for soil sampling from every tree species and diameter class as three replications. All of soil samples were excavated in north aspect and at the nearest point to tree collar for more precision. Soil samples were taken at 0-15, 15-30 and 30-45cm depths using auger soil sampler with 81cm2 cross section. The result of this research showed that bulk density was significantly greater under beech than under hornbeam. This character tends to be less in 0-15cm depth than in 15-30cm and 30-45cm depths. Variable amounts of this character were found among diameter classes of beech and hornbeam also. Silt and clay were significantly greater under hornbeam than under beech. Moisture was significantly higher under beech than under hornbeam, whereas soil depths and diameter classes did not show any significant difference. Current research has shown that the influence of individual trees with different diameter classes can be detected in forest floors and upper minerals soil layers even under mixed stands in steepy sloping landscapes. This subject should be considered in natural forests management. Key words: Bulk density, Hyrcanian forest, moisture, old trees, soil texture

INTRODUCTION Tree-soil interactions and their influence on tree fitness and forest community dynamics are complex. Many current theories on spatial heterogeneity and species diversity of forest communities are based on the premise that species interaction is controlled by competition for resources such as light, water, nutrients (Binkley and Menyailo 2005). Although these resources are largely constrained by the physical environment, the influence of canopy trees on resources can be of significant importance in forest ecosystem dynamics. This biotic control over resources has received little attention until recently in understanding forest ecosystem dynamics. Several authors have demonstrated the existence of a close interaction between plant and soil (Lovett et al. 2002; Compton et al. 2003; Templer et al. 2005). The evidence above suggests that tree-soil feedbacks need to be incorporated into the concept of species diversity and spatial heterogeneity in forest ecosystems in order to gain more insight in long-term forest dynamics. The soil under the influence of a forest develops properties that vary spatially with relation to the location of the trees. This variation in soil properties is frequently reflected in the distribution of the various

species of the ground flora. The amelioration or degradation of the forest soil takes place with each tree as a center of influence (Kooch et al. 2011). Individual species are an important control on soil properties such as structure, water availability, and biota, as well as nutrient cycling. Tree species may influence soil nutrient cycling directly, via nutrient uptake (Turner et al. 1993), litter inputs (Prescott 2002), and induced leaching losses (Compton et al. 2003; Templer et al. 2005), and indirectly, via alteration of microclimate and disturbance regime (Chapin et al. 2002), precipitation chemistry and floral and faunal activities (Smolander and Kitunen 2002). Studies of trees grown in monocultures effectively isolate species effects on soils, but may not adequately capture species effects in mixed stands (Rothe and Binkley 2001). Despite continued research into tree species effects on soil nutrient cycles, the generality of these effects remains unknown (Binkley and Menyailo 2005). For example, leaf litter decomposition experiments have shown that mixtures of litter of different species can exhibit additive, neutral, and antagonistic effects on overall decomposition that are not easily predicted from the characteristics of the individual litters alone (Gartner and Cardon 2004). More generally, experimental studies of

B I O D I V E R S IT A S 14 (1): 25-30, April 2013

grasslands have shown that species diversity and functional characteristics can impact a range of ecosystem processes that serve as the context for individual species effects on soils (Tilman et al. 2001). Thus, plants can shape long-term patterns of soil and ecosystem development (Jenny 1941) in ways that may affect subsequent interspecific interactions and plant-soil relationships. Old-growth forests of northern Iran provide a unique opportunity to examine tree species-soils relationships in a wide range of mixedspecies ecosystems that developed with minimal anthropogenic disturbance. Northern forests of Iran stretch up to an altitude of 2800 m asl. and comprise different forest types with 80 species of trees and shrubs. There is 1.9×106 ha of hardwood forests in the north of Iran, which is called Hyrcanian ecosystem (Hosseini et al. 2007; Rouhi-Moghaddam et al. 2008; Poorbabaei and Poorrostam 2009). The Hyrcanian forests are one of the last remnants of natural deciduous forests in the world (Sagheb Talebi 2000). Beech (Fagus orientalis Lipsky) is one of the most important elements of forests in the temperate broad-leaf forest biome and represents an outstanding example of the re-colonization and development of terrestrial ecosystems and communities after the last ice age, a process which is still ongoing (Mosadegh 2000; Marvie Mohadjer 2007). In the north of Iran, pure and mixed oriental beech forests cover 17.6 per cent of the surface land area and represent 30 per cent of the standing volume. Beech is the most valuable wood-producing species in the Caspian forests (Resaneh et al. 2001). The beech trees are found in small groups up to 500m asl. while individuals have been reported from 110m up to 2650m. At low altitudes, they occur mixed with hornbeam (Carpinus betulus L.) (Marvie

Mohadjer 2007). In spite the important of Hyrcanian forests, but earlier study that has evaluated the effects of dominated individual trees on soil characters at the stand level wasn't considered. The objective of this study is to quantify the effects of beech and hornbeam single tree species on soil physical indicators in an old-growth hardwood forest of Iran that is the first survey in these forests.

MATERIALS AND METHODS Site description This research was conducted in Experimental Forest Station of Tarbiat Modares University located in a temperate forest of Mazandaran province in the north of Iran, between 36˚ 31’ 56˝ N and 36˚ 32‘ 11˝ N latitudes and 51˚ 47‘ 49˝ E and 51˚ 47‘ 56˝ E longitudes (Figure 1). The maximum elevation is 1700m and the minimum is 100m. Minimum temperature in December (6.6˚C) and the highest temperature in June (25˚C) are recorded, respectively. Mean annual precipitation of the study area were from 280.4 to 37.4 mm at the Noushahr city metrological station, which is 10Km far from the study area. For performing this research, a limited area of reserve parcel (relatively undisturbed) considered that was covered by Fagus orientalis and Carpinus betulus dominant stands. This limitation had an inclination 60-70 percent with northeast exposure at 546-648 m asl. Bedrock is limestonedolomite with silty-clay-loam soil texture. Presence of logged and bare roots of trees is indicating rooting restrictions and soil heavy texture (Kooch et al. 2010).

Experimental Forest Station of Tabiat Modares University

Islamic Republic of Iran

Figure 1. Location of the study site inside the Hyrcanian zone, the Central Caspian region of northern Iran.

KOOCH et al. – Soil characteristics of beech and hornbeam trees habitat

Soil sampling Due to examine the influence of forest individual trees on soil physical indicators, twenty hectare areas of Experimental Forest Station of Tarbiat Modares University was considered. The positions of trees with diameter at breast height (DBH) (1.3 m) more than 45 cm (Goodburn and Lorimer 1999; Scahrenbroch and Bockheim 2007; Kooch et al. 2011) were recorded by Geographical Position System (GPS). Three single-trees (was defined as trees with canopy cover separated from other trees and covered distinguished space) considered for soil sampling from every tree species and diameter class as three replications. All of soil samples were excavated in north aspect and at the nearest point to tree collar for more precision. Soil samples were taken at 0-15, 15-30 and 30-45cm depths using auger soil sampler with 81cm2 cross section (Kooch et al. 2011). Laboratory analyses For this purpose, large live plant material (root and shoots) and pebbles in each sample were separated by hand and discarded. The air-dried soil samples were sieved (aggregates were crushed to pass through a 2 mm sieve) to remove roots prior to analysis. Bulk density at air dried moisture content was measured by Plaster (1985) method (clod method). Soil texture was determined by the Bouyoucos hydrometer method (Bouyoucos 1962). Soil moisture was measured by drying soil samples at 105° C for 24 hours (Ghazanshahi 1997). Statistical analyses Normality of the variables was checked by KolmogrovSmirnov test and Levene test was used to examine the equality of the variances. Differences between diameter classes and depths in soil properties were tested with twoway analysis (ANOVA) using GLM procedure, with diameter classes (45-55, 55-65, 65-75, 75-85, 85-95, 95105cm) and depth (0-15, 15-30 and 30-45 cm) as independent factor. Interactions between independent factors were tested also. Duncan test was used to separate the averages of the dependent variables which were

significantly affected by treatment. Independent sample ttest carried out for compare means of soil properties between beech and hornbeam single trees. Significant differences among treatment averages for different parameters were tested at P ≤ 0.05. SPSS v. 11.5 software was used for all the statistical analysis.

RESULTS AND DISCUSSION Analysis of variance of studied characters is indicating that in relation to beech single trees, the greater amounts of bulk density belong to 45-55cm diameter class and the least was detected in 65-75cm class (Table 1). This character showed the maximum and minimum in 45-55cm and 7585cm diameter classes, respectively under hornbeam trees (Table 2). Bulk density was significantly greater under beech than under hornbeam (Figure 2). This character tends to be less in 0-15cm depth than in 15-30cm and 30-45cm depths (Tables 1 and 2). Soil texture components showed no significantly difference among diameter classes of beech trees, but the greater amounts of silt content was found in 30-45cm depth (Table 1). Under hornbeam, the higher values of silt, clay and lower amounts of sand were considered in 75-85 diameter class (Table 2). Sand content was significantly higher in 0-15cm, whereas the greater amounts of silt detected in 30-45cm depth. Clay amounts did not show any significant difference between depths (Table 2). Silt and clay were significantly greater under hornbeam than under beech (Figure 2). Moisture was significantly higher under beech than under hornbeam (Figure 2), whereas soil depths and diameter classes did not show any significant difference (Tables 1 and 2). Results of present research are indicating that individual trees can be effective on soil physical indicators. The weight of a tree, combined with the movement of structural roots during windy conditions, can compress soils over centimeter-scales (Chappell et al. 1996). With considering to mountainous position of Hyrcanian forests in Iran and presence of trees with high diameters (old trees), therefore, it is imagined that many of trees are influenced by

Table 1. Mean of soil physical indicators in relation to diameter classes and soil depth in beech site Variable / soil character Diameter class (cm)

Bulk density (g/cm3)

Sand (%)

Silt (%)

Clay (%)

Moisture (%)

45-55 1.13 (0.00)a 33.19 (0.59) 37.66 (0.31) 29.15 (0.28) 40.30 (0.27) 55-65 1.11 (0.00)bc 32.04 (0.63) 38.72 (0.41) 29.23 (0.29) 39.54 (0.29) 65-75 1.10 (0.00)c 32.11 (0.67) 38.61 (0.41) 29.27 (0.28) 41.82 (0.26) 75-85 1.12 (0.00)b 32.00 (0.64) 38.72 (0.41) 29.27 (0.28) 39.93 (0.30) 85-95 1.11 (0.00)bc 32.11 (0.67) 38.61 (0.41) 29.27 (0.28) 39.24 (0.29) 95-105 1.12 (0.00)ab 33.18 (0.58) 37.66 (0.31) 29.15 (0.28) 39.88 (0.30) F-value 7.60** 0.70ns 2.14ns 0.02ns 2.23ns Soil depth (cm) 0-15 1.11 (0.00)b 32.94 (0.41) 37.78 (0.22)b 29.27 (0.19) 40.21 (0.21) 15-30 1.12 (0.00)a 32.71 (0.39) 38.07 (0.20)b 29.21 (0.19) 39.89 (0.22) 30-45 1.12 (0.00)a 31.68 (0.48) 39.13 (0.31)a 29.18 (0.19) 40.26 (0.70) F-value 10.50** 1.90ns 7.86** 0.03ns 0.21ns Interaction 0.70ns 0.09ns 0.38ns 0.00ns 0.77ns Note: ** Different is significant at the 0.01 level. (ns): Non significant differences (P > 0.05). Values are the means ±St. error of the mean (in parenthesis). Within the same column the means followed by different letters are statistically different (P < 0.05).

B I O D I V E R S IT A S 14 (1): 25-30, April 2013

Table 2. Mean of soil physical indicators in relation to diameter classes and soil depth in hornbeam site Bulk density (g/cm3)

Variable / soil character

Sand (%)

Silt (%)

Clay (%)

Moisture (%)

45-55 1.13 (0.00)a 33.18 (0.58)a 37.26 (0.31)c 29.15 (0.28)b 39.40 (0.33) 55-65 1.12 (0.00)a 32.04 (0.63)ab 38.73 (0.41)b 29.23 (0.29)b 39.18 (0.30) 65-75 1.09 (0.00)b 30.31 (0.66)b 39.57 (0.45)b 30.11 (0.28)b 39.76 (0.28) 75-85 1.05 (0.00)c 25.34 (1.89)c 42.53 (1.85)a 32.07 (0.29)a 39.89 (0.32) 85-95 1.11 (0.01)ab 30.27 (0.67)b 39.57 (0.45)b 30.16 (0.28)b 39.41 (0.29) 95-105 1.11 (0.00)ab 32.00 (0.64)ab 38.73 (0.41)b 29.27 (0.28)b 39.32 (0.27) F-value 13.89** 17.08** 24.79** 11.10** 0.70ns Soil depth (cm) 0-15 1.09 (0.00)c 31.92 (0.51)a 37.97 (0.21)c 30.07 (0.32) 39.85 (0.21) 15-30 1.10 (0.00)b 30.97 (0.58)a 39.02 (0.30)b 29.99 (0.31) 39.42 (0.19) 30-45 1.11 (0.00)a 28.68 (1.23)b 41.38 (0.95)a 29.93 (0.31) 39.21 (0.20) F-value 4.43* 12.34** 54.87** 0.08ns 2.07ns Interaction 0.35ns 3.95** 16.39** 0.00ns 0.27ns Note: ** Different is significant at the 0.01 level. *Different is significant at the 0.05 level. (ns): Non significant differences (P > 0.05). Values are the means ±St. error of the mean (in parenthesis). Within the same column the means followed by different letters are statistically different (P < 0.05).

1.12

t = 2.93 Sig = 0.00

1.11 1.1

1.09 Beech

33 32.5 32 31.5 31 30.5 30 29.5

40 t = 3.34 Sig = 0.00

Beech

28.5 Beech

38.5

Hornbeam

Moisture (%)

Clay (%)

29.5 29

37.5

30.5 30

Hornbeam

t = - 3.66 Sig = 0.00

t = - 2.68 Sig = 0.00

39.5 Silt (%)

1.13 Sand (%)

Bulk density (gr/cm3)

Diameter class (cm)

40.2 40 39.8 39.6 39.4 39.2 39

Beech

Hornbeam

t = 2.22 Sig = 0.00

b Beech

Hornbeam

Figure 2. Mean of soil physical indicators in relation to beech and hornbeam individual trees

windthrow event. Old trees in study area (beech and hornbeam) with high diameters and intensive crown covering are similar to sail in front of windthrow, therefore, are more impacted of heavy windthrow. The factors collection together including large crowns and full foliage, rooting form, the higher height and high diameters of these trees making theirs vulnerable to windrthrow (Kooch et al. 2008). Thus, heavy windthrow can be imposed on these trees and are due to theirs movement in small scale that this subject is effective on variability of bulk density. At the millimetre scale, the growth of tree roots can locally increase the density of soil and have a localized impact on bulk density (Blevins et al. 1970; Whalley et al. 2004). Thus, mentioned factors can be effective on variability of bulk density under individual trees. In this research, bulk

density increased in soil deeper layers. Both living and decayed roots can create well-connected pores in the topsoil called ‘macropores’ (Chandler and Chappell 2008). Pay attention to upper soils have more density of fine roots, thus these pores occurred in superficial soils that are due to decreasing of bulk density, finally. Bulk density showed significantly increasing under beech than hornbeam. Soil acidification due to an increase in the rate of dissolution of soil minerals beneath trees (Augusto et al. 2000), acidic litter-fall (Chappell et al. 2006) or acidic exudates (Chappell et al. 2007) has been shown to reduce soil structural stability. This reduced stability can lead to a reduction in soil porosity. High rates of leaching by infiltrating stem-flow can exacerbate the acidification effect (Augusto et al. 2002). Regarding to low acid under

KOOCH et al. â&#x20AC;&#x201C; Soil characteristics of beech and hornbeam trees habitat

beech than hornbeam, thus instability is more considered in soils imposed by beech trees. By this reason, porosity is decreased under beech and bulk density will be increased that is according to obtained result in this research. The soil acidity also affects the presence and abundance of soil fauna, such as earthworms (Neirynck et al. 2000). As earthworm activity creates more stable soil aggregates and adds macro-porosity, reduced abundance would be expected to increase of bulk density. In general, soil pH detected as the most important effective factor on earthworms abundance (Boettcher and Kalisz 1991; Neirynck et al. 2000). Research results of Kooch et al. (2011) in study area showed that soil pH was significantly less under beech than hornbeam and earthworm's abundance were fewer also. Thus bulk density showed significantly increasing under beech than hornbeam. This result also can be related to more activity of earthworm's population under hornbeam individual trees. The composition of the over story has an impact on soil structure (Read and Walker 1950). Graham and Wood (1991), Graham et al. (1995) have shown that the soil structure and its stability were tree species dependent, probably because of differential effects on worm activity. Furthermore, wild and domesticated animals use isolated trees for shelter during rainstorms or for shade from intense solar radiation. This congregation of animals, particularly at times when the soil is wet, can compact the soil and thereby increase the bulk density of the soil horizon (Drewry et al. 2000). Regarding to more amounts of moisture under beech than hornbeam, soil compaction was more occurred, thus increasing of bulk density is more considered. Silt and clay were more gathered under hornbeam than beech that can be related to earthworm's greater densities as with creation of macropores they are due to changes in the components of soil texture. Earthworms are able to transferring of smaller components of soil (i.e. clay and silt) to different layers. Beech individual trees with superficial rooting system have more ability for preservation of soil moisture in upper soil. Thus, moisture was significantly higher under beech than under hornbeam, whereas soil depths did not show any significant difference. In total, compared to open areas, the reduced precipitation received beneath tree canopies due to enhanced wet-canopy evaporation (David et al. 2006) combined with greater root abstraction to support transpiration can lead to considerably greater topsoil drying during rain-free periods (Ziemer 1968; Katul et al. 1997). The study has shown that the influence of individual trees with different diameter classes can be detected in forest floors and upper minerals soil layers even under mixed stands in steepy sloping landscapes. The magnitude of the differences observed depends to some degree on the nature of the forest stand and under story vegetation and on climatically and topographically controlled processes such as litter redistribution and soil creep. In any case, the soil landscape may be viewed as a mosaic, with properties of the individual pedons composing the mosaic reflecting the occurrence and physical characteristics of the tree species present. Differences in substrate properties beneath the crown of juxtaposed tree species may in some cases be

large enough to result in short-range variations in soil properties and plant growth (Kooch et al. 2011). Present research was the first survey to quantify the local effect of individual trees on soil physical indicators in Hyrcanian forests of Iran. However, the effect of over story species is strongly influenced by forest management (e.g. low density stands or mixed stands) that, further researches should address this point.

CONCLUSION The forest soils can be strongly influenced by tree species. Many studies have addressed the effects of monocultures on forest soil physical, but few have examined the effects of varying ratios of species within stands. In current research, the validity of the concept of "single-tree influence circles" was tested in a forest dominated by beech (Fagus orientalis Lipsky) and hornbeam (Carpinus betulus L.) on steep slopes in the Alborz Mountain, Hyrcanian forest of Iran. In this paper, we presented data on and discussed the effects of individual species trees on soil physical indicators in a single soil map unit in an old-growth northern hardwood forest. Soil bulk density and moisture were significantly greater under beech than under hornbeam. Whereas, silt and clay were significantly greater under hornbeam than under beech. We propose that soil diversity in this oldgrowth northern hardwood forest is substantial and suggest that it be considered in soil survey and forest management.

REFERENCES Augusto L, Ranger J, Binkley D, Rothe A. 2002. Impact of several common tree species of European temperate forests on soil fertility. Ann For Sci 59: 233-253. Binkley D, Menyailo OV. 2005. Gaining insights on the effects of tree species on soils. In: Binkley D, Menyailo OV. (eds). Tree species effects on soils: Implications for global change. Springer, New York. Blevins RL, Holowaychuk N, Wilding LP. 1970. Micromorphology of soil fabric at tree root-soil interface. Soil Sci Soc Amer J 34: 460-465. Boettcher SE, Kalisz PJ. 1991. Single-tree influence on earthworms in forest soils in Eastern Kentucky. Soil Sci Soc Amer J 55: 862-865. Bouyoucos GJ. 1962. Hydrometer method improved for making particle size analysis of soils. Agron J 56: 464-465. Chandler KR, Chappell NA. 2008. Influence of individual oak (Quercus robur) trees on saturated hydraulic conductivity. For Ecol Manag 256: 1222-1229. Chapin FSI, Matson PA, Mooney HA. 2002. Principles of terrestrial ecosystem ecology. Springer, New York. Chappell N, Stobbs A, Ternan L, Williams A. 1996. Localised impact of Sitka Spruce (Picea sitchensis (Bong) Carr.) on soil permeability. Pl Soil 182: 157-169. Chappell NA, Tych W, Bonell M. 2007. Development of the for SIM model to quantify positive and negative hydrological impacts of tropical reforestation. For Ecol Manag 251: 52-64. Chappell NA, Vongtanaboon S, Jiang Y, Tangtham N. 2006. Return-flow prediction and buffer designation in two rainforest headwaters. For Ecol Manag 224: 131-146. Compton JE, Church MR, Larned ST, Hogsett WE. 2003. 2-fixing red alder. Ecosystems 6: 773-785. David TS, Gash JHC, Valente F, Pereira JS, Ferreira MI, David JS. 2006. Rainfall interception by an isolated evergreen oak tree in a Mediterranean savannah. Hydrol Process 20: 2713-2726.

B I O D I V E R S IT A S 14 (1): 25-30, April 2013

Drewry JJ, Littlejohn RP, Paton RJ. 2000. A survey of soil physical properties on sheep and dairy farms in southern New Zealand. New Zealand J Agric Res 43: 251-258. Gartner TB, Cardon ZG. 2004. Decomposition dynamics in mixed-species leaf litter. Oikos 104: 230-246. Ghazanshahi J. 1997. Soil and plant analysis. Homa Publ, Tehran. Goodburn JM, Lorimer CG. 1999. Population structure in old-growth and managed northern hardwoods: an examination of the balanced diameter distribution concept. For Ecol Manag 118: 11-29. Graham RC, Wood HB. 1991. Morphologic development and clay redistribution in hypsometer soils under Chaparral and Pine. Soil Sci Soc Amer J 55: 1638-1646. Graham RC, Ervin JO, Wood HB. 1995. Aggregate stability under oak and pine after four decades of soil development. Soil Sci Soc Amer J 59: 1740-1744. Hosseini SM, Kartoolinejad D, Mirnia SK, Tabibzadeh Z, Akbarinia M, Shayanmehr F. 2007. The effects of Viscum album L. on foliar weight and nutrients content of host trees in Caspian Forest (Iran). Polish J Ecol 55: 579-583. Jenny H. 1941. Factors of soil formation: a system of quantitative pedology. McGraw-Hill, New York. Katul G, Todd P, Pataki DE, Kabala ZJ, Oren R. 1997. Soil water depletion by oak trees and the influence of root water uptake on the moisture content spatial statistics. Water Res Res 33: 611-623. Kooch Y, Hosseini SM, Akbarinia M. 2008. The ecological effects of pit and mounds created by a windthrow on understory of Hyrcanian forests. J Silva Balcanica 9: 13-28. Kooch Y, Hosseini SM, Mohammadi J, Hojjati SM. 2010. The effects of gap disturbance on soil chemical and biochemical properties in a mixed beech-hornbeam forest of Iran. Ecologia Balkanica 2: 39-56. Kooch Y, Hosseini SM, Mohammadi J, Hojjati SM. 2011. Analysis of earthworm's patchy distribution and variability of soil biochemical properties under single-tree influences. Intl J Environ Sci 1: 18131829. Lovett GM, Weathers KC, Arthur MA. 2002. Control of nitrogen loss from forested watersheds by soil carbon: nitrogen ratio and tree species composition. Ecosystems 5: 712-718. Marvie Mohadjer MR. 2007. Silviculture. Tehran Univ Publ, Tehran. Mosadegh A. 2000. Silviculture. Tehran Univ Publ, Tehran. Neirynck J, Mirtcheva S, Sioen G, Lust N. 2000. Impact of Tilia platyphyllos Scop., Fraxinus excelsior L., Acer pseudoplatanus L., Quercus robur L., and Fagus sylvatica L. on earthworm biomass and physico-chemical properties of a loamy topsoil. For Ecol Manag 133: 275-286.

Plaster EJ. 1985. Soil science and management. Delmar Publ Inc., Albany, NY. Poorbabaei H, Poorrostam A. 2009. The effect of shelterwood silvicultural method on the plant species diversity in a beech (Fagus orientalis Lipsky) forest in the north of Iran. J For Sci 55: 387-394. Prescott CE. 2002. The influence of the forest canopy on nutrient cycling. Tree Physiol 22: 1193-1200. Read RA, Walker LC. 1950. Influence of eastern redcedar on soil in Connecticut pine plantations. J For 23: 337-339. Resaneh Y, Moshtagh MH, Salehi P. 2001. Quantitative and qualitative study of north forests. In Nation seminar of management and sustainable development of north forests, Ramsar, Iran, August 2000, Jehad-e Agriculture Ministry, Forests and Ranges Organization Press. Vol. 1: 55-79. Rothe A, Binkley D. 2001. Nutritional interactions in mixed species forests: a synthesis. Canadian J For Res 31: 1855-1870. Rouhi-Moghaddam E, Hosseini SM, Ebrahimi E, Tabari M, Rahmani A. i. Comparison of growth, nutrition and soil properties of pure stands of Quercus castaneifolia and mixed with Zelkova carpinifolia in the Hyrcanian forests of Iran. For Ecol Manag 255: 1149-1160. Sagheb Talebi Kh. 2000. Hyrcanian forests (North of Iran), the unique ecosystem in near east region, in proceeding, XXI world congressForests and Society: The role of research, Kuala Lumpur, 13-15 August 2000. Scahrenbroch BC, Bockheim JG. 2007. Pedodiversity in an old-growth northern hardwood forest in the Huron Mountains, Upper Peninsula, Michigan. Canadian J For Res 37: 1106-1117. Smolander A, Kitunen V. 2002. Soil microbial activities and characteristics of dissolved organic C and N in relation to tree species. Soil Biol Biochem 34: 651-660. Templer PH, Lovett GM, Weathers KC, Findlay SE, Dawson TE. 2005. Influence of tree species on forest nitrogen retention in the Catskill Mountains, New York, USA. Ecosystems 8: 1-16. Tilman D, Reich PB, Knops JM, Wedin DA, Mielke T, Lehman C. 2001. Diversity and productivity in a long-term grassland experiment. Science 294: 843-845. Turner DP, Sollins P, Leuking M, Rudd N. 1993. Availability and uptake of inorganic nitrogen in a mixed old-growth coniferous forest. Pl Soil 148: 163-174. Whalley WR, Leeds-Harrison PB, Leech PK, Risely B, Bird NRA. 2004. The hydraulic properties of soil at root-soil interface. Soil Sci 169: 90-99. Ziemer RR 1968. Soil moisture depletion patterns around scattered trees. Research Note PSW-166. US Forest Service, Berkeley.

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 31-36

ISSN: 1412-033X E-ISSN: 2085-4722 DOI: 10.13057/biodiv/d140105

Species composition of understory vegetation in coal mined land in Central Bengkulu, Indonesia WIRYONOâ&#x2122;Ľ, ARIF BUHA SIAHAAN Department of Forestry, Faculty of Agriculture, University of Bengkulu. Jl. Raya Kandang Limun, Bengkulu 38371A, Bengkulu, Indonesia. Tel.: +62-736-21170; Fax.: +62-736-21290; ď&#x201A;Šemail: wiryonogood@yahoo.com.

Manuscript received: 28 February 2013. Revision accepted: 26 April 2013.

ABSTRACT Wiryono, Siahaan AB. 2013. Species composition of understory vegetation in coal mined land in Central Bengkulu, Indonesia. Biodiversitas 14: 31-36. Coal strip mining in forest area has destroyed forest ecosystem and created barren land. Reclamation of mined land is done by revegetating the land. In addition to planted species, pioneer species usually grow naturally in mined land. The objectives of this study were to know the species composition of understory vegetation growing naturally in coal mined land planted with Gmelina arborea in Central Bengkulu, Indonesia, and to compare that composition with that of unreclaimed coal mined land and of natural forests. Data were collected by sampling understory vegetation in study site. Each plant was identified, harvested and oven-dried to find the biomass. Results showed that the reclaimed mined land had 16 understory species from 6 families, and the abandoned mined land had 10 species from 3 families, lower than that of natural forests, which were 92 and 112. The three most important species were Scleria sumatrensis Retz, Eragrostis chariis (Schult.) Hitchc and Paspalum conjugatum Berg. The species composition of understory vegetation in reclaimed mined land had high similarity with that of abandoned mined land but was totally different from that of natural forests. Key words: Coal mined land, understory, species diversity

INTRODUCTION Coal is one of fossil fuels widely used in Indonesia. Coal strip mining commonly conducted in forest area in Indonesia has destroyed the natural forest and created barren land. In general, mined soils have physical, chemical and biological problems that may inhibit optimal plant growth (Bradshaw 1997; Lottermoser 2010). The use of heavy machinery and the high content of rock have resulted in highly compacted soil material, impeding root penetration (Bussler et al. 1984). Chemically, many mined lands have low pH, leading to the increase of soluble iron, aluminum and zinc ions that may cause toxicity to plants. Mined land has low organic matter and soil organisms (Gould and Liberta 1981). Efforts have been done to overcome this low fertility. Physically, soil compaction can be reduced by ripping, tilling, or contouring to improve aeration and infiltration (Ashby 1997; Jacinthe and Lal 2007). Chemically, soil acidity is alleviated by liming (Bradshaw 1997). Biologically, mined land may be introduced with mycorrhiza (Cordell et al. 1999), Rhizobium (Widyati 2007) or earthworms (Vimmerstedt and Finey 1973; Nurliana and Wiryono 2004). Naturally, succession will bring back the composition of vegetation of mined land into its original one, but it takes very long time. In Western Australia, Norman et al. (2006) found that vegetation composition of mined land had not reached the original state after it had been

revegetated for 14 years. Chaffey and Grant (2000) found similar situation in Tomago, New South Wales, Australia. Previous studies in North America also showed the slow process of succession in mined land (Glen-Lewin 1979; Jonescu 1979). To speed up the succession, deliberate restorations of mined land have been done. Restoration of degraded land may be viewed as reconstruction of original ecosystem (Cooke and Johnson 2002), but there is an argument whether this is desirable or possible due to the dynamic nature of ecosystem and the irrevesibility of some changes that might have happened (Hobbs and Harris 2001). Revegetation of mined land is an early step to bring back the original ecosystem. However, due to the low soil fertility of the land, the species planted are usually the pioneer ones which can grow in harsh condition. In Sumatra, several pioneer species have been successfully planted in mined land such as Paraserianthes falcataria, Leucaena leucocephala, Sesbania grandiflora, and Acacia mangium (Munawar 2003; Nurliana and Wiryono 2004; Suhartoyo et al. 2012). Several pioneer shrub species have been used to improve soil chemical, physical and biological properties of mined land in Bengkulu (Prawito 2009). Litter from pioneer vegetation can improve soil nutrient for plants in mined land (Munawar et al. 2011). In addition to planted species, some pioneer species naturally invade the area. Both the planted and naturally invading species will undergo succession and the

B I O D I V E R S IT A S 14 (1): 31-36, April 2013

community will finally reach the climax. Community structure and species composition are some factors to be considered in determining the success of ecosystem restoration (Tongway and Ludwig 2006; Cooke and Johnson 2002). The objectives of this research were to know the species composition of understory (Br: understorey) plants growing naturally in coal mined land recently revegetated with Gmelina arborea in Central Bengkulu, Indonesia, and to compare it with that of abandoned or unrevegetated coal mined land and of natural forests.

MATERIALS AND METHODS Site and time This research was done in coal mining area of Danau Mas Hitam Company in Taba Penanjung Sub District, Central Bengkulu District, Bengkulu Province (Figure 1), Indonesia, in May-July 2008. Before mining the site used to be hill forest in the Bukit Barisan Mountain range, with altitudes of 300-500 m above sea level. It has wet climate with an average annual rainfall approximately 3,000 mm. Sampling Samplings of ground cover vegetation and soil were done in two types of mined lands, namely the reclaimed land planted with Gmelina arborea 1.5 years before the sampling and one abandoned (un-reclaimed) mined land. The reclaimed mined land was introduced with mycorrhiza

and Rhizobium by another researcher. This revegetated land consisted of two sites having different soil colors. The first site was strong brown (7.5 YR 4/6 in Munsell soil color charts) and the other was black (5Y 2.5/1). The abandoned land had dark yellowish brown (10 YR Âž) soil materials. We did not investigate the cause of color differences among sites. Samplings of vegetation were done in 1 x 1 m plots with 25% sampling intensity. The number of sample plots in strong brown reclaimed soils was 63, in black reclaimed soil 72 and in abandoned mined soil 135. The plots were placed systematically with random start. For every plot, each species of understory plants consisting of herbs and shrubs less than 2 m in height were recorded, harvested and placed in paper bags. Harvest method was used because this method can give better quantitative data than percent coverage method. The bags were then oven-dried at a temperature of 105o C for 24 hours or more until the weight was constant. For identification, a specimen of herbarium was taken for each species. These specimens were oven-dried at a temperature of 80 o C for 8 hours. A composite soil sample was taken from each land type. The soil samples were then dried and taken to Soil Laboratory in the Faculty of Agriculture, the University of Bengkulu, for chemical and physical analyses. Chemical analyses were done to find out the pH, and nitrogen, phosphor, and potassium content. Physical analyses were done to determine the soil porosity.

Figure 1. Location of study (yellow mark), in the Sub-district of Taba Penanjung, Central Bengkulu District, Bengkulu Province, Indonesia.

WIRYONO & SIAHAAN – Understory vegetation in coal mined land

Data analyses Plant species identification was conducted in the Herbarium of Forestry Department, University of Bengkulu, using several field guides (Soerjani et al. 1987; Sastrapradja and Afriastini 1980, 1981; Hafliger and Scholz 1980, 1981; Hafliger et al. 1982). Species importance was determined by biomass, because clumped grasses and creeping plants constituted a large portion of understory plants in the study site. It is not possible to count individual stem of grasses in clumps and of creeping plants. According to Whittaker (1975) species importance in a community can be determined by several quantitative measurements, one of which is biomass. This study did not use percent coverage method, because visual estimate of coverage would give less accurate data than actual weighing of the biomass. Biomass for each plant, calculated using the formula in Brower et al. (1998): Bi = Wi A

Bi = Biomass of i species (g.m-2) ΣWi = Dry weight of all individuals of i species (g) A = Area sampled (m2) To compare the composition of each land, Sørensen Index of Similarity was calculated (Mueller-Dombois and Ellenberg 1974). Sørensen Index: ISS =

2c x 100 % A B

A = the number of all species found in in A community B = the number of all species found in B community c = the number of common species (found in both A and B)

land was much lower than those in natural forests in Bengkulu, which were 92 in Bukit Kaba (Loanita 1999) and 112 in Lebong Selatan Sub District (Setiawan, 1998). In this present study, species diversity index was not determined because it is not possible to count the number of plants of clumped grasses and creeping plants. Number of species is the simplest measurement of species diversity (Whittaker, 1975). Colinvaux (1986) even believed that number of species is more meaningful than diversity index. Table 1. Species composition of understory vegetation in coal mined land of Danau Mas Hitam Company in Taba Penanjung Sub District, Central Bengkulu District. Species

Family

A1 A2 B

Chromolaena odorata (L.) Asteraceae + + + R.M.King & H.Robinson Mikania micrantha H.B.K. Asteraceae + + + Wedelia trilobata L Asteraceae + + Porophyllum ruderale (Jacq.) Cass. Asteraceae - + + Imperata cylindrica (L.) P. Beauv. Poaceae + + Paspalum commersonii Lamk. Poaceae + + + Paspalum conjugatum Berg. Poaceae + + + Pennisetum sp. Poaceae - + Eragrostis chariis (Schult.) Hitchc. Poaceae + + + Eleusine indica (L.) Gaertn. Poaceae + + + Pycreus sanguinolentus (Vahl) Nees Cyperaceae - + + Scleria sumatrensis Retz. Cyperaceae + + + Fimbristylis miliaceae (L.) Vahl Cyperaceae - + Polygala paniculata. L. Polygalaceae + + Calopogonium mucunoides Desv. Fabaceae - + Hyptis rhomboidea Mart. & Gal. Lamiaceae - + Mimosa pudica L. Fabaceae + + Number of species 11 16 10 Note : (+) Present ; (-) Absent; Land A1 = strong brown reclaimed land; Land A2 = black reclaimed; Land B = abandoned land. Family: Asteraceae = Compositae, Poaceae = Gramineae Lamiaceae = Labiateae

Data of understory plants of natural forest were taken from the theses of Loanita (1999) in Bukit Kaba, Kepahiang District and Setiawan (1998) Lebong Selatan, Lebong District, both in Bengkulu Province, within the radius of 50 km.

RESULTS AND DISCUSSION Species composition The understory vegetation in mined land was composed of 17 species, from 7 families. The black reclaimed soil had the highest number of species, 16, while the dark brown reclaimed soil had only 11 species, almost the same with the non reclaimed land which had 10 species (Table 1; Figure 2). The number of species in this mined land was higher than 4-year old vegetation in another mined in Muara Enim, South Sumatra, which was only 10 (Suhartoyo et al. 2012). The species richness of this mined

Figure 2. The number of species (S) of understory plant in strong brown reclaimed mined land (A1), black reclaimed mined land (A2) and abandoned mined land (B).

B I O D I V E R S IT A S 14 (1): 31-36, April 2013

Table 3. The biomass of understory plants in three types of mined land. Species

Figure 3. Biomass (g.m-2) of understory vegetation in strong brown reclaimed mined land (A1), black reclaimed mined land (A2) and abandoned mined land.

The low species richness of understory vegetation in mined land was presumably caused by two factors. First, the land was only recently reclaimed or abandoned. In Western Australia, Norman et al. (2006) found that the composition of vegetation in mined land had not matched that of the original vegetation, even after 14 years of reclamation.Similar situation was found in Tomago, New South Wales (Chaffey and Grant 2000). The second factor may be the low fertility of the mined land as shown by soil test results (Table 2), indicating that all sites in general had low soil fertility. Table 2. Soil pH, nitrogen, phosphorus and potassium content, and porosity

Land types Dark brown reclaimed land (A1) Black reclaimed land (A2) Abandoned land (B)

NKTotal pHP 2O 5 total available porosity H 2O (%) (ppm) (me.100g-1) (%) 4.3 0.16 3.21 0.1 48.605 4.5

0.14 4.33

0.3

45.402

4.2

0.13 5.16

0.41

46.281

Note: ppm = part per million, me = milli equivalent.

Species importance Species importance was determined by the biomass. The three most important or dominant species were Scleria sumatrensis, Eragrostis chariis, and Paspalum conjugatum, but they ranked differently in each land type (Table 3). In dark brown reclaimed land, the biomass of Scleria sumatrensis and Eragrostis chariis had much higher biomass than the other species. Scleria sumatrensis is a perennial grass, has dense clumps, and may reach 2m in height (Nasution 1986). A clump of this species may cover 1 m2 of ground. Eragrostis chariis can grow in compacted stony soil, sandy soil, or clay. It has extensive and deep root system so that it is hard to uproot. It may reach 1.25 in height and it has many leaves near the ground (Sastrapradja and Afriastini 1981). It was obvious that the two grasses were capable of producing large biomass and could therefore dominate the areas.

Biomass (g.m-Â˛) A1 A2 B 92.76 7.26 1.59 19.07 2.52 1.79 1.39 10.75 1.35 1.14 1.41 0.43

Scleria sumatrensis Retz. Eragrostis chariis (Schult.) Hitchc. Paspalum conjugatum Berg. Chromolaena odorata (L.) R.M.King & H.Robinson Eleusine indica (L.) Gaertn. 0.02 0.02 Mikania micrantha H.B.K. 0.43 0.01 Paspalum commersonii Lamk. 0.58 0.33 Mimosa pudica L. 1.40 0.13 Wedelia trilobata 0.11 0.27 Polygala paniculata. L. 0.06 0.28 Imperata cylindrica (Linn.) P. Beauv. 0.57 0.33 Fimbristylis miliaceae (L.) Vahl 0 0.44 Hyptis rhomboidea Mart. & Gal. 0 0.13 Calopogonium mucunoides Desv. 0 5.46 Pycreus sanguinolentus (Vahl) Nees 0 0.22 Porophyllum ruderale (Jacq.) Cass. 0 0.09 Pennisetum sp. 0 0 Total 117.54 29.63 Note: Land A1 = strong brown reclaimed land; Land A2 reclaimed land; Land B = abandoned land.

0.02 0.10 0.22 0 0 0 0 0 0 0 0.46 0.03 0.09 6.07 = black

In the black reclaimed soil, Paspalum conjugatum was the most dominant species, with much higher biomass than the other species. This species grows well in open space (Nasution 1986) as in this type of land. This species has strong root system and may reach 50 cm in height and has 3-5 leaves in each node. It reproduces by seeds as well as by rhizome. Even in hard soil this species thrives (Sastrapradja and Afriastini 1980). The biomass of reclaimed land was much higher than that of abandoned land (Figure 3). This might be due to the introduction of mycorrhiza and nitrogen fixing bacteria and fertilization in the reclaimed land. Although both the reclaimed and abandoned mined land had low fertility, it is possible that mycorrhiza and Rhizobium which might have infected the roots help the plants take nutrients from the soil. It has been reported the addition of both Rhizobium and mycorrhiza can increase the uptake of nitrogen, phosphorus and potassium by seedlings to be used for rehabilitation of mined land (Widyarti 2007). Reforestation of coal mined land in Ohio was successful due to inoculation of mycorrhiza (Cordell et al. 1999). Composition similarity SĂ&#x2DC;rensenâ&#x20AC;&#x2122;s Index (Table 4) showed that both reclaimed mined had high similarity, which was 81%. This means that the species composition of both areas was relatively the same. Both reclaimed land had moderately high (63%, and 69%) similarity index with abandoned mined land. When the composition of each mined land type was compared with that of natural forests in Bukit Kaba (Loanita 1999) and in Lebong Selatan Sub District (Setiawan 1998), the indices showed zero values, meaning that the species composition of understory vegetation in mined land was totally different from that in natural forest. The presence of indigenous species is one of nine criteria

WIRYONO & SIAHAAN – Understory vegetation in coal mined land

for the success of restoration set by the Society of Ecological Restoration (Clewel and Aronson 2007). This total difference indicated that mined land and natural forest had different stage of succession. Mined land vegetation was in the early stage of succession while natural forest was in a climax stage, or in late stage of succession. The species colonizing the mined land were pioneer species. Over time, these species will be gradually replaced by late succession species. In South Sumatra, even after 15 years of mined reclamation, the species composition of ground cover was still different from that of the natural forest nearby (Suhartoyo et al. 2012). In Australia, the rehabilitated mined land, age 8-24 years, only had 12-37 species in common with the adjacent natural shrub land (Herath et al. 2009).

abandoned mined land. The species composition of two types of reclaimed mined land was similar to each other and to that and abandoned mined land, but totally different from that of natural forests.

Table 4. Species composition similarity of understory vegetation among land types

REFERENCES

Types of land compared Strong brown reclaimed land and black reclaimed mined land Strong brown reclaimed land and abandoned mined land Black reclaimed land and abandoned mined land Reclaimed mined land and natural forest Abandoned mined land and natural forest Note: ISs = SØrensen’s Index of Similarity,

ISs (%) 81.15 63.64 69.23 0 0

Soil properties The soil properties (Table 2) in reclaimed and abandoned mined land showed low fertility (Balai Penelitian Tanah 2005). All three sites were very acidic and had low total nitrogen. Potassium levels were low in both reclaimed land and medium in abandoned land. The difference, however, was very little. Phosphorus levels were very low in reclaimed land and low in abandoned land. The porosity was medium for all sites. The sites had low fertility because the soil surface material was not top soil, but mine spoil. The presence of vegetation for one year had not increased soil fertility. Other studies in Sumatra also showed that newly reclaimed coal mined had relatively low soil fertility (Suhartoyo et al. 2012; Munawar 2003; Nurliana and Wiryono 2004). The soil condition in this study site was not extremely harsh; so many species of pioneer plants invaded this site naturally. Some mine sites are so harsh that only few plants can grow unless soil amelioration has been conducted (Bradshaw 1997).

CONCLUSION The understory vegetation in coal mined land under 1.5 year-old Gmelina arborea stand was composed of 16 species of plants from 6 families. The abandoned mined land had only 10 species from 3 families. The three most important species were Scleria sumatrensis Retz, Eragrostis chariis (Schult.) Hitchc and Paspalum conjugatum Berg. The biomass of understory vegetation in reclaimed mined land was much higher than that of

ACKNOWLEDGEMENTS We thank the management of Danau Mas Hitam Company who allowed us to do research in their concession area. We appreciate the help and suggestion of Guswarni Anwar during our research. The valuable suggestions from an anonymous reviewer are gratefully acknowledged.

Ashby WC. 1997. Soil ripping and herbicides enhance tree and shrub restoration on stripmines. Restor Ecol 5:169-177. Balai Penelitian Tanah. 2005. Chemical analyses for soil, plants, water and fertilizers. Research and Development Agency, The Minstry of Agriculture, Jakarta [Indonesian] Bradshaw AD. 1997. The importance of soil ecology in restoration science. In Urbanska, KM , Webb NR , Edwards PJ (eds) Restoration ecology and sustainable development. Cambridge University Press, UK. Brower JE, Zar JH, von Ende CN. 1998. Field and laboratory methods for general ecology. 4th ed. WCB McGraw-Hill. Boston. Massachusetts. Bussler BH, Byrness WR, Pope PE, Chaney WR. 1984. Properties of minesoil reclaimed for forest land use. Soil Sci Soc Amer J 48:178184. Chaffey CJ, Grant CD. 2000. Fire management implications of fuel loads and vegetation structure in rehabilitated sand mines near Newcastle, Australia. For Ecol Manag 129:269-278. Clewel AF, Aronson J. 2007). Ecological restoration. Principles, values and structure of an emerging profession. Island Press, Washington, D.C. Colinvaux P. 1986. Ecology. John Wiley & Sons, New York. Cooke JA, Johnson MS. 2002. Ecological restoration of land with particular reference to the mining of metals, and industrial minerals: A review of theory and practice. Environ Rev 10:41-71. Cordell CE, Marrs LF, Farley ME. 1999. Mycorrhizal fungi and trees—a successful Reforestation alternative for mine land reclamation. In Vories KC, Throgmorton D (eds) Proceedings of Enhancement of reforestation at surface coal mines: Technical interactive forum. Drawbridge Inn and Conference Center Fort Mitchell, Kentucky March 23-24, 1999. U.S. Department of the Interior, Office of Surface Mining, Coal Research Center, Southern Illinois University, Carbondale, Texas Utilities. Glen-Lewin DC. 1979. Natural revegetation of acid coal spoils in Southern Iowa. In M.K. Wali (ed) Ecology and coal resources development. Pergamon Press, New York. Gould AR, Liberta AE. 1981. Effects of storage during surface mining on the viability of vesicular arbuscular mycorrhiza. Mycologia 73:914922. Hafliger E, Scholz H. 1980. Grass Weeds 1. CIBA-GEIGY. Switzerland. Hafliger E, Scholz H. 1981. Grass Weeds 2. CIBA-GEIGY. Switzerland. Hafliger E, Kuhn U, Hame L, Cook, CDK, Faden R, Speta F. 1982. Monocot weeds 3. CIBA-GEIGY. Switzerland. Herath DN, Lamont BB, Enright NJ, Miller BP. 2009. Comparison of post-mine rehabilitated and natural shrubland communities in Southwestern Australia. Rest Ecol 17 (5): 577-585 Hobbs RJ, Harris JA. 2001. Restoration ecology. Repairing the earth’s ecosystem in the new millennium. Rest Ecol 9 (2): 239-246. Jacinthe, PA, Lal R. 2007. Carbon storage and minesoil properties in relation to topsoil applications techniques. Soil Sci Soc Amer J 71: 1788-1795. Jonescu, ME. 1979. Natural revegetation of strip-mine land in the lignite and coal fields of Western Saskatchewan. In: Wali MK (ed) Ecology and coal resources development. Pergamon Press, New York.

B I O D I V E R S IT A S 14 (1): 31-36, April 2013

Loanita L. 1999. Analysis of understory vegetation of Bukit Kaba hill forest. [Thesis] Department of Forestry, University of Bengkulu, Bengkulu [Indonesian]. Lottermoser BG. 2010. Mine Wastes. Characterization, treatment and environmental impacts. 3rd ed. Springer. Berlin. Mueller-Dumbois D, Ellenberg H. 1974. Aims and methods in vegetation ecology. John Willey & Sons, New York. Munawar A. 2003. Soil fertility levels in coal mined soil in two-year-old stands of Paraserianthes falcataria L. and Sebania grandiflora Pers. Jurnal Lembaga Penelitian Universitas Bengkulu 4 (7):1-5. [Indonesian]. Munawar A, Indramawan, Suhartoyo H. 2011. Litter production and decomposition rate in the Reclaimed Mined Land under Albizia and Sesbania stands and their effects on some soil chemical properties. J Trop Soils (16) 1: 1-6. Nasution U. 1986. Weeds and their control in rubber plantation in North Sumatra and Aceh. The Center for Research and Development of Plantation at Tanjung Morawa, Medan. [Indonesian]. Norman MA, Koch JM, Grant CD, Morald TK, Ward SC. 2006. Vegetation succession after bauxite mining in Western Australia. Restoration Ecology 14: 278-288. Nurliana S, Wiryono. 2004. The effects of surface soil treatments on the growth of Sesbania grandiflora and Leucaena leucocephala in coal mined soil. Jurnal Penelitian UNIB 10 (3): 145-149. [Indonesian]

Prawito P. 2009. The use of pioneer species in the rehabilitation process of post mined land in Bengkulu. Jurnal Ilmu Tanah dan Lingkungan 9 (1):7-12. [Indonesian] Sastrapradja S, Afriastini JJ. 1980. Species of low landgrasses Biologi Nasional. LIPI. Bogor. [Indonesian] Sastrapradja S, Afriastini JJ. 1981. Species of mountainous grasses. Lembaga Biologi Nasional_LIPI. Bogor. [Indonesian] Setiawan I. 1998. Analysis of understory vegetation of Kerinci Seblat National Park in Tes, Lebong Selatan Sub-district. [Thesis]. Department of Forestry, University of Bengkulu, Bengkulu. Soerjani M, Kosterman AJGH, Tjitrosoepomo G. 1987. Weeds of rice in Indonesia. Balai Pustaka. Jakarta. Suhartoyo H, Munawar A, Wiryono. 2012. Returning biodiversity of rehabilitated forest on a coal mined site at Tanjung Enim, South Sumatra. Biodiverstas 13:13-17. Tongway DJ, Ludwig JA. 2006. Assessment of landscape function as an information source for mine closure. In A. Fourie A, Tibbet M (eds) Mine Closure. Australian Centre for Geomechanics, Perth. Vimmerstedt JP, Finney JH. 1973. Impact of earthworm on litter burial and nutrient distribution in Ohio strip mine spoil banks. Soil Sci Soc Amer J 37: 388-393. Whittaker RH. 1975. Communities and Ecosystems. 2-nd ed. MacMillan Publishing Co. Inc. New York. Widyati E. 2007. Formulation of microbe inoculums: MA, BPF and Rhizobium from coal mined soil for seedlings of Acacia crassicarpa Cunn. Ex-Benth. Biodiversitas 8 (3): 238-241.

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 37-42

ISSN: 1412-033X EISSN: 2085-4722 DOI: 10.13057/biodiv/d140106

Proposing local trees diversity for rehabilitation of degraded lowland areas surrounding springs SOEJONO1,♥, SUGENG BUDIHARTA1, ENDANG ARISOESILANINGSIH2 1

Purwodadi Botanic Garden, Indonesian Institute of Sciences, Jl. Raya Surabaya-Malang, Km.65 Purwodadi, Pasuruan, East Java, Indonesia. Tel./fax: +62-341-426046, email: soejono59@gmail.com 2 Department of Biology, Faculty of Mathematics and Natural Sciences, Brawijaya University, Malang 65145, Indonesia Manuscript received: 14 November 2012. Revision accepted: 24 March 2013.

ABSTRACT Soejono, Budiharta S, Arisoesilaningsih E. 2013. Proposing local trees diversity for rehabilitation of degraded lowland areas surrounding water spring. Biodiversitas 14: 37-42. This study was aimed to propose alternative trees diversity for rehabilitation of degraded lowland area surrounding spring. Data were collected by vegetation analysis of three sampling sites (1st. Cowek, 2nd Gajahrejo, 3rd Parerejo) to determine density, frequency, dominancy, diversity index and Important Value Index (IVI). The lists of plants in three sites were then compiled into an integrated list and used as reference for developing questionnaire. The questionnaire was then distributed to respondents who were chosen randomly. We recorded their preferences of tree species in rehabilitation program based on socio-economical and ecological aspects. Selected species were then proposed as alternative plants for rehabilitation of degraded spring area based on landscape topography and remaining vegetation coverage. The results showed that species diversity of Moraceae family was the highest than other families. In term of ecological aspect, Ficus racemosa, Artocarpus elasticus, Bambusa blumeana, Dendrocalamus asper, Gigantochloa atter, Ficus benjamina, Syzygium samarangense and Ficus virens showed high Important Value Index. On the other hand, based on socio-economic aspects, Ficus benjamina, Artocarpus elasticus, Artocarpus altilis, Artocarpus altilis “Seedless”, Durio zibethinus, Ficus drupacea, Pangium edule, Ficus variegata, Michelia champaca, Aleurites moluccana and Ficus racemosa were the most preferred species by local community. Based on topography and vegetation coverage, spring surrounding areas were classified into four: steep and open, flat and open, steep and dense, and flat and dense. Therefore among of 120 species found in all sampling sites, there were respectively 63.3%, 95%, 25% and 44.16% species to be proposed and planted for rehabilitation in the four classified areas. Key words: Tree diversity, rehabilitation, degraded areas, spring

INTRODUCTION The impacts of habitat degradation are not only decreasing plant and animal species diversity, but also accelerating threatens ecological processes and natural resources in short and long term, including declining water quality and flow rate. It is known that water is an important product of ecosystem services to humans, and its quality and quantity depends on many factors; among them are the carrying capacity of physical environment and quality of vegetation coverage in the catchment area of spring. Therefore, conservation of plants diversity and ecosystems, both in situ, ex situ and rehabilitation of degraded areas is ecological significant value. Various efforts to rehabilitate degraded lands and forests in Indonesia held using diverse ways or scenarios by the parties, but in general they often plant and prioritize exotic trees species, especially plant for timber production purposes, such as acacia (Acacia mangium), sengon (Albizia falcataria) and jabon (Anthocephalus cadamba) (Nawir et al. 2007). These plants will not grow long because it will be harvested to provide for wood needs, so the impact of rehabilitation for the urgent purposes such as sustainable environmental improvements and or ecological

service is poorly integrated. In addition, not all rehabilitated sites are ecologically, socially and economically suitable to be planted using limited species richness as well as exotic ones, whereas, fault the plants choice for rehabilitation, will lead to counter-productive results. Some researchers showed that in the areas successfully reforested with pine, residents complained that the well water was shrinking (Sumarwoto 2003). Yonky et al. (2003) mentioned that pine has a high value of evaporation (1000-2500 mm year-1 ) depend on the location and climate condition. It will cause water deficit in the watershed, especially if it is planted in areas where rainfall is less than 2000 mm year-1. However, in areas with high rainfall (3308 mm year-1) as in Somagede, Sempor, Kebumen, where they studied, the pine forest is not cause of water shortages in the downstream. Controversy about this is still often discussed, because pine is an exotic and plant providing not only for reforestation, but also expected to support the success of business revenues, from wood and resin products (Yonky et al. 2003). On the other hand, planting exotic plant, Acacia nilotica in Baluran, is expanding rapidly. This plant is then known to be invasive type (Hernowo 1999; Sabarno 2001; Iskandar 2006; Zuraida 2011), so its control becomes a significant

B I O D I V E R S IT A S 14 (1): 37-42, April 2013

problem. Djufri (2004) stated that the invasion of Acacia nilotica has resulted in the reduction of savanna in Baluran National Park reaching 50%. Pressure to the savanna showed a great impact on the balance and preservation of whole ecosystem in Baluran. Therefore this study was aimed to propose plant diversity for rehabilitation degraded lowland area surrounding spring.

MATERIALS AND METHODS This study was conducted in three sites in the subdistricts Purwodadi, Pasuruan, East Java (Figure 1). Information of spring locations was obtained from the local people. Data were collected in three sites (1st Cowek, 2nd Gajahrejo, 3rd Parerejo) for vegetation analysis using Mueller-Dombois and Ellenbergâ&#x20AC;&#x2122;s method as noted in (Soerianegara and Indrawan 1983) in order to determine density, frequency, dominancy, diversity index and Important Value Index. Eleven plots of 1ha square shape were observed for each site. The lists of plants in three sites were then compiled into one integrated list and used as reference for developing questionnaire. The questionnaires

were then distributed to respondents chosen randomly in order to record data on local community preferences in selecting tree species, viewed from social and economic aspects. Selecting tree species to be proposed for rehabilitation degraded lowland areas surrounding water spring was conducted based on some criteria, such as (i) ecological (altitude requirement, pioneer-climax species, and fast or slow growing species, local or exotics), (ii) socio-economic aspects (wood or non wood products) and (iii) clustering degraded area by topography (flat or slope) and existing vegetation coverage (absence or presence of coverage). Based on topography and vegetation coverage, spring surrounding areas were classified into four: steep and open, flat and open, steep and dense, as well as flat and dense. Using these criteria, suitability of tree species was determined using a rapid assessment and expert judgment, based on field observations and records of empirical knowledge. This paper is an output of a thematic subprograms research activity of Purwodadi Botanical Gardens in 2011/2012, entitled, Study of vegetation and rehabilitation of habitats surrounding spring in Pasuruan district, East Java, Indonesia.

Gajahrejo

Parerejo

Cowek

D Figure 1. Research study sites: A. Indonesia, B. East Java province, C. Pasuruan district, D. Purwodadi subdistricts with three study sites, i.e.: 1. Cowek, 2. Gajahrejo and 3. Parerejo, each consists of 11 plots

SOEJONO et al. â&#x20AC;&#x201C; Proposing plant diversity for rehabilitation

Table 1. Vegetation profile at three sampling sites around lowland spring in Districts Purwodadi, Pasuruan (Soejono and Budiharta 2011, modified) Variable

1st Cowek

No. of families No. of genus No. of species Dominant family Diversity index Co-dominant species and (% IVI)

30 28 55 37 72 69 Moraceae Moraceae 5.08 5.06 Ficus racemosa (29.4), Bambusa blumeana (53.9), Ceiba pentandra (23.6), Dendrocalamus asper (41.2), Artocarpus elasticus (18.1), Ceiba pentandra (26.6), Swietenia macrophylla (16.8), Gigantochloa atter (15.4), Ficus virens (16.8). Ficus benjamina (5.3). 64 110

RESULTS AND DISCUSSION Ecological aspects At least there were 120 species of trees growing in habitat around the lowland springs. It is known that the family Moraceae found as the highest species diversity than others, such as Ficus racemosa, also reached the highest importance value index in the first site Cowek, while Bambusa blumeana showed the highest importance value index in the second and third sites (Table 1). Trees species reached high Importance Value Index (IVI) including Ficus racemosa, Artocarpus elasticus, Bambusa blumeana, Dendrocalamus asper, Gigantochloa atter, Ficus benjamina, Ficus virens and Syzygium samarangense. The average density of trees in the three sites were still relatively low, 64, 110 and 80 trees per ha. Lieberman and Lieberman (1994) reported the results of their research that the total number of stems â&#x2030;Ľ 10 cm dbh, enumerated in 12.4 ha, a mean density is 446.0 individuals ha-1. This information is useful for determining tree density and species diversity existing in these sites, and then for estimating seedling density requirement for rehabilitation or restoration of degraded areas by considering their ecological and functional approach. According to Manan (1992), the best approach to restore diversity or for rehabilitation of degraded land was using the adjacent natural community structure (primary forests) as a vegetation model, especially in complexity, composition, vertical or horizontal stratification, richness, diversity and endemism rate. Consequently, the result of the succession acceleration by rehabilitation would be optimal as expected and harmony under natural conditions. In general, the more diverse plant species and structure, the better its effect on soil and water conservation. Socio-economic aspects Survey was carried out to record data on community preferences, involved 60 respondents from three sampling sites. In general, the results of survey showed that the species of Moraceae was a widely accepted by local communities for rehabilitation purpose of degraded areas around the spring. The high level of preference of

3rd Parerejo

All sites

23 42 54 Moraceae 4.5 Bambusa blumeana (91.4), Syzygium samarangense (25.7), Ceiba pentandra (21.9), Ficus virens (15.4), Dendrocalamus asper (12.9). 80

33 78 120 Moraceae

84.8

respondents to the diverse species of Moraceae indicated that traditional knowledge on plant species commonly grown around the spring is still preserved and it is in harmony with the ecological aspects. Besides Moraceae, respondents preferred local tree species producing various economical benefits such as Durio zibethinus, Pangium edule, Parkia timoriana, Aleurites moluccana, Artocarpus altilis, Artocarpus elasticus as a producer of fruits or seeds, while Cananga odorata and Michelia champaca as a producer of aromatic flowers. Examples of selected plants for rehabilitation of open area around the spring and socioeconomic reason by local people are listed in Figure 2.

Pl an t s sp ec ie s

Density (ind. ha-1)

2nd Gajahrejo

Figure 2. Some local tree species selected by local people for rehabilitation of open area around the spring and providing socioeconomic benefits

From Figure 2, it showed that diversity of tree species of the family Moraceae was higher than other families, consist of two genera and covering seven species (Artocarpus elasticus, A. altilis and Ficus benjamina, F. drupacea, F. variegata, F. virens and F. racemosa). Moraceae is a member of flowering plants, tribe Rosales.

B I O D I V E R S IT A S 14 (1): 37-42, April 2013

Potential tree species diversity for rehabilitation based on two criteria: topography and existing vegetation cover Analysis of promising tree species based on topography and existing vegetation cover, implemented by a rapid assessment (judgment), field observations and records of empirical knowledge of the researcher team of Purwodadi Botanical Gardens, who often carry out field exploration in various remote tropical primary rain forest and also supported by main literature (Backer and Bakhuizen 1965 1968; Heyne 1987; Soerianegara and Lemmens 1994; Soejono 2011; Narko et al. 2012). Landscape around the spring was divided into four simple groups based on topography and existing vegetation: steep and open area (absence of trees coverage), flat and open, steep and dense (presence of dense trees), and flat and dense. Therefore among of 120 species found in all sampling sites, it was noted that: 63.3%, 95%, 25% and 44.16% respectively were proposed to be planted for rehabilitation in the four classified areas. Some examples of tree species proposed for rehabilitation in the mentioned classified areas, are listed in Table 2.

Adenanthera pavonina L. Aleurites moluccana (L.) Willd. Arenga pinnata (Wurmb) Merr. Artocarpus altilis (Park.) Fosberg Artocarpus elasticus Reinw.ex Blume. Artocarpus heterophyllus Lkm. Baccaurea dulcis (Jack.) Mull. Arg. Bambusa blumeana J.A. and J.H.Schultes Cananga odorata (Lmk) Hook.f.& Thoms. Dendrocalamus asper (Schult.) Backer ex Heyne) Dracontomelon dao (Blanco)Merr.& Rolfe Dysoxylum gaudichaudianum ( A.Juss) Miq. Durio zibethinus Murr. Ficus benjamina L. Ficus callosa Willd. Ficus drupacea Thunb. Ficus hispida L. f. Ficus variegata Blume Ficus kurzii King Ficus virens W. Aiton Ficus racemosa L. Litsea glutinosa (Lour.) C.B. Rob. Gigantochloa apus (Bl. Ex Schult.f.) Kurz Gigantochloa atter (Hassk.) Kurz ex Munro Microcos tomentosa J.E. Smith. Michelia champaca Linn. Protium javanicum Burm f. Pangium edule Reinw. Parkia timoriana (DC.) Merr. Pterocymbium javanicum R. Br. Pterospermum javanicum Jungh. Sterculia foetida L. Syzygium pycnanthum Merr. and L.M. Perry Syzygium cumini (L.) Skeels Terminalia microcarpa Decne

● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●

● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●

Flat and dense

Species

Steep and dense

Table 2. Some examples of tree species showed a great potential for rehabilitation in the classified areas Flat and open

Using a simple technology, seed germination and seedling growth of Ficus benjamina, F. drupacea, F. racemosa, F. variegata and F. virens were successfully propagated by seeds (Soejono 2007). Main character of this genus was shown in the fruit namely figs. The fruit is formed from the base of the enlarged flowers and closed to form orbicular. The flowers are hidden inside the figs. The important thing to note that the most of Moraceae grown in lowland tropics, even, some species of the genus of Ficus, estimated that its distribution centered located in the Indo-Malay region, includes Indonesia. Some Ficus species are also known to be classified as a keystone species, because fruits are favored by wildlife as food. Therefore, these species show a great potential, if planted as a material for environmental remediation (Sastrapradja and Afriastini 1984; Berg and Corner 2005; Widyatmoko and Irawati 2007). In accordance to the restoration and control of water resources, some species of Ficus show positive characteristics, such as, grow deep and broad rooting system, produce a dense branching in low position, develop a broad canopy, that are potential to reduce speed of rainfall drops. Thus destructive force to the surface layer of top soil is lower, and the water infiltration to the ground is better. As a result, water is retained relatively longer in the soil and released slowly, allowing the continuity of spring and reduce erosion or landslides (Soejono 2011). Yulistyarini and Sofiah (2011) stated that quality of various environmental services was depended on the density and diversity of vegetation, soil type and its management. They mentioned that, the high diversity of vegetation and thickness of litter will maintain hydrological function of recharge area and protect flow of water spring. Bruijnzeel 1990 mentioned that environmental carrying capacity in the water supply decreased, primarily due to changes in vegetation coverage, related to change in the pattern of evapotranspiration, infiltration rate, and the quality and quantity of surface flow. While Primack (1998) states that some important points in restoring degraded land community, mostly relies on community efforts to reestablish native plants, because this plant community usually produces most biomass and able to provide the structure for other community members. Robinson and Johnson (2006) state that appropriate plant materials for restoration by selecting species that are suitable for the site, grow from locally adapted sources, and have a solid genetic composition contribute to the success of project. In line with this discussion, Bohnen and Galatowitsch (2005) stated that in most cases, high species diversity is recommended for restoration to increase ecological function. The first preference is typically for seed and plants that come from similar site conditions, and as close to the restoration site as possible. Edwards et al. (2010) introduced restoration model to support sustainable livelihoods – building both environmental and social resilience to climate change in the Shire Valley. They combined selected three multi-purpose species, Jatropha, neem and Moringa to spread risks and provide quick diverse benefits.

Steep and open

● ● ● ● ● ● ●

● ● ● ● ● ● ● ●

● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●

● ● ● ● ● ● ● ●

●

SOEJONO et al. â&#x20AC;&#x201C; Proposing plant diversity for rehabilitation

Tree species selection mentioned above, should also consider ecological suitability in more detailed, including soil type, texture, structure and depth, climate, water use efficiency, as well as and autoecology of each species. Furthermore, the plant diversity for rehabilitation of degraded lowland areas surrounding spring was proposed by improving conventional replanting process using single species, and considering different perspectives, such as preserving plants diversity, prioritizing selection of local species, considering the ecological and socio-economic function, appreciating community preferences and adjusting to the local areas conditions. Hopefully, this proposes can technically implementable, ecologically sustainable, economically profitable, socially acceptable and can be developed in other places with similar conditions. Cooperation and commitment In fact the success of rehabilitation in degraded areas is not only determined by scientific considerations, but also determined by the result of mutual cooperation and commitment of all parties. To create synergies and optimize the collective efforts in biodiversity conservation management, Donald (2013) reported that management action needed to be enriched by research and allowed researchers to learn from practitioners. In the implementation of its activities, it is important to coordinate with relevant agencies, landowners and apply certain approaches or and dissemination to the public. Moreover, planted seedlings for rehabilitation are also required regularly protection and maintenance in early step until plants able to adapt to its environment.

CONCLUSION It can be concluded that there were 120 species of local trees found in three sampling sites. Among them showed great potential as multipurpose plants and nominated by local people as material for rehabilitation of degraded lowland areas surrounding spring. Furthermore, this alternative plant diversity for rehabilitation may improve conventional replanting process using single species, and consider different perspectives, such as preserving plants diversity, prioritizing selection of local species, consider the ecological and socio-economic function, appreciate community preferences, adjust to the local areas conditions and finally establish cooperation with various parties. Hopefully, this propose can be developed in other places with similar conditions for optimal and sustainable ecological services of spring.

REFERENCES Backer CA, Bakhuizen van den Brink Jr. RC. 1965. Flora of Java Vol. II. N.V.P. Noordhoff, Groningen, The Netherlands. Backer C.A, RC. Bakhuizen van den Brink Jr. 1968. Flora of Java Vol. III. N.V.P. Noordhoff, Groningen, The Netherlands. Berg CC, EJH Corner. 2005. Flora Malesiana Series I-Seed Plants Vol 17/ Part 2-2005, Moraceae (Ficus). National Herbarium Nederland, Leiden.

Bohnen JL, Galatowitsch SM. 2005. Spring peeper meadow: revegetation practices in a seasonal wetland restoration in Minnesota. Ecol Restor 23: 172-181. Bruijnzeel, LA. 1990. Hydrology of Moist Tropical Forests and Effects of Conversion: A State of Knowledge Review. UNESCO, Paris. Djufri. 2004. Acacia nilotica (L.) Willd. ex Del. and problematical in Baluran National Park, East Java. Biodiversitas 5 (2): 96-104

[Indonesia] Edwards K, Chimusoro J, Davidson G, Price K, Abbot P, Kayambazinthu D. 2010. Restoring degraded land in the Shire Valley, Malawi: lessons for community led initiatives that link restoration and the development of sustainable livelihoods. 18th Commonwealth Forestry Conference, Edinburgh. 28 June - 2 July 2010. Yonky I, Rahardyan NA, Sukresno. 2003. The role of Hydrograph Analysis for Overcoming Water Conflicts in Society: A Case Study Sub Das Silengkong and Watujali BKPH (Section of the Forest Management Unit) Karanganyar, KPH (Forest Management Unit) South Kedu. Proceedings of the National Workshop Towards Ecosystem-Based Regional Resource Management to reduce the potential of inter-communal conflict. [Indonesia] Hernowo JB. 1999. Habitat and local distribution of Javan Green Peafowl (Pavo muticus muticus Linneaus 1758) in Baluran National Park, East Java. Media Konservasi 6 (1): 15-22. Heyne K. 1987. Useful plants of Indonesia (Translation). Forestry Research and Development Agency. Jakarta. [Indonesia] Iskandar S. 2006. The efforts to against the forest invasive species in Indonesia; A review. Country Paper, Presented To The Workshop On Development Of A Strategy For The Asia-Pacific Forest Invasive Species Network. Dehradun, India, 16 April 2006. Lieberman M, Lieberman D. 1994. Patterns of density and disperson of forest trees. La Silva: Ecology and Natural History of a Neotropical Rain Forest Part II Chap 8. hydro.csumb.edu/lieberman/docs/Density and dispersion chap 8 La Selva book.pdf Manan S. 1992. Silviculture. In: Kadri W (ed). Manual of Forestry. Indonesian Ministry of Forestry. Jakarta. [Indonesia] McDonald T. 2013. Optimising our collective efforts-one step forward. Ecol Manag Rest 14 (1). DOI: 10.1111/emr.12032. Narko D, Suprapto A, Lestarini W. 2012. An alphabetical list of plant species cultivated in the Purwodadi Botanic Garden. Purwodadi Botanic Garden, Indonesian Institute of Sciences. Pasuruan. Nawir AA, Murniati, Rumboko L. 2007. Forest rehabilitation in Indonesia: Where to after more than three decades. Center for International Forestry Research (CIFOR). Bogor, Indonesia. Primack RB. 1998. Conservation Biology. Yayasan Obor Indonesia. Jakarta. [Indonesia] Robinson BW, Johnson R. 2006. Selecting native plant material for restoration projects. Extension Service, Oregon State University. OR. Sabarno MY. 2001. Baluran savanna and its conservation efforts. Proceedings of the National Seminar on Biodiversity Conservation and Utilization of Dry Land Plant. Purwodadi Botanical Garden, Indonesian Institute of Sciences, Pasuruan [Indonesia] Sastrapradja S, Afriastini JJ. 1984. Relatives of banyan. Series of Natural Resources 115. National Institute of Biology-LIPI. Bogor [Indonesia] Soejono. 2007. Successful generative propagation of Golden Fig (Ficus bejamina L.) in Purwodadi Botanic Garden. Proceedings International Seminar Advances in Biological Science: Contribution Toward a Better Human Prosperity. Faculty of Biology, Gajah Mada University, Yogyakarta. Soejono, Budiharta S. 2011. Ecological aspects and socio-economic preferences of local communities into species selection for water spring habitat rehabilitation: Case study in Purwodadi, Pasuruan. Proceeding International Conference on Biological Science Faculty of Biology Universitas Gadjah Mada 2011. ICBS BIO-UGM 2011). Soejono. 2011. The trees species diversity around spring at two areas in Purwodadi, Pasuruan. Proceeding International Conference On Biological Science Faculty of Biology Universitas Gadjah Mada 2011 (ICBS BIO-UGM 2011). Soemarwoto. 2003. Forests, afforestation/reforestation and water. Kompas, October 20, 2003. [Indonesia] Soerianegara I, Indrawan A. 1983. Indonesian forest ecology. Department of Forest Management, Faculty of Forestry, Bogor Agricultural University. Bogor. [Indonesia] Soerianegara I, Lemmens RHMJ. 1994. Timber Trees: Major Commersial Timbers Trees 5(1) Plant Resources of South-East Asia. Prosea Foundation, Bogor.

B I O D I V E R S IT A S 14 (1): 37-42, April 2013

Widyatmoko D, Irawati. 2007. Dictionary of terms conservation. Center Plant Conservation Bogor Botanical Gardens. Indonesian Institute of Sciences, Bogor. [Indonesia]

Yulistyarini T, Sofiah S. 2011. Valuing quality of vegetation in recharge area of Seruk Spring, Pesanggrahan Valley, Batu City, East Java. Biodiversitas 12 (4): 229-234 Zuraida. 2011. Potency of Acacia nilotica as invasive species at Baluran National Park, East Java-Indonesia. Indian J Ecol 38: 216-217.

B I O D I V E R S IT A S Volume 14, Number 1, April 2013 Pages: 43-53

ISSN: 1412-033X E-ISSN: 2085-4722 DOI: 10.13057/biodiv/d140107

Review: Current trends in coral transplantation – an approach to preserve biodiversity MOHAMMED SHOKRY AHMED AMMAR1,♥, FAHMY EL-GAMMAL2, MOHAMMED NASSAR2, AISHA BELAL2, WAHID FARAG2, GAMAL EL-MESIRY2, KHALED EL-HADDAD2, ABDELNABY ORABI2, ALI ABDELREHEEM2, AMGAD SHAABAN2 1

National Institute of Oceanography and Fisheries (NIOF), Hydrobiology Department, P.O. Box 182, Suez, Egypt. Tel. +20 11 1072982, Fax. +20 623360016, e-mail: shokry_1@yahoo.com. 2 National Institute of Oceanography and Fisheries (NIOF), P.O. Box 182, Suez, Egypt. Manuscript received: 13 February 2013. Revision accepted: 29 March 2013.

ABSTRACT Ammar MSA,El-Gammal F, Nassar M, Belal A, Farag W, El-Mesiry G, El-Haddad K, Orabi A, Abdelreheem A, Shaaban A. 2013. Review: Current trends in coral transplantation – an approach to preserve biodiversity. Biodiversitas 14: 43-53. The increasing rates of coral mortality associated with the rise in stress factors and the lack of adequate recovery worldwide have urged recent calls for actions by the scientific, conservation, and reef management communities. This work reviews the current trends in coral transplantation. Transplantation of coral colonies or fragments, whether from aqua-, mariculture or harvesting from a healthy colony, has been the most frequently recommended action for increasing coral abundance on damaged or degraded reefs and for conserving listed or “at-risk” species. Phytoplanktons are important for providing transplanted corals with complex organic compounds through photosynthesis. Artificial surfaces like concrete blocks, wrecks or other purpose-designed structures can be introduced for larval settlement. New surfaces can also be created through electrolysis. Molecular biological tools can be used to select sites for rehabilitation by asexual recruits. Surface chemistry and possible inputs of toxic leachate from artificial substrates are considered as important factors affecting natural recruitment. Transplants should be carefully maintained, revisited and reattached at least weekly in the first month and at least fortnightly in the next three months. Studies on survivorship and the reproductive ability of transplanted coral fragments are important for coral reef restoration. A coral nursery may be considered as a pool for local species that supplies reef-managers with unlimited coral colonies for sustainable management. Transplanting corals for making artificial reefs can be useful for increasing biodiversity, providing tourist diving, fishing and surfing; creating new artisanal and commercial fishing opportunities, colonizing structures by fishes and invertebrates), saving large corals during the construction of a Liquified Natural Gas Plant. Key words: Coral transplantation, biodiversity, aquaculture, mariculture, nursery, artificial reefs

INTRODUCTION Coral reefs are underwater structures made from calcium carbonate secreted by corals. They are also colonies of tiny living animals found in marine waters that contain few nutrients. Most coral reefs are built from stony corals, which in turn consist of polyps that cluster in groups. Coral reefs are fragile ecosystems, partly because they are very sensitive to water temperature. They face numerous threats from climate change, oceanic acidification, blast fishing, cyanide fishing for aquarium fish, overuse of reef resources, and harmful land-use practices, including urban and agricultural runoff and water pollution, which can harm reefs by encouraging excess algal growth. The coral reef ecosystem is a diverse collection of species that interact with each other and the physical environment. The sun is the initial source of energy for this ecosystem. Through photosynthesis, phytoplankton, algae, and other plants convert light energy into chemical energy. As animals eat plants or other animals, a portion of this energy is passed on. The Importance of corals and coral reefs include: (i) Corals remove and recycle carbon dioxide.

Excessive amounts of this gas contribute to global warming. (ii) Reefs shelter land from harsh ocean storms and floods. (iii) Reefs provide resources for fisheries. Food items include fishes, crustaceans, and mollusks. (iv) Coral reefs attract millions of tourists every year. (v) The coral reef is an intricate ecosystem and contains a diverse collection of organisms. Without the reef, these organisms would die. (vi) Some evidence suggests that the coral reef can potentially provide important medicines, including anti-cancer drugs and a compound that blocks ultraviolet rays. (vii) Coral skeletons are being used as bone substitutes in reconstructive bone surgery. The pores and channels in certain corals resemble those found in human bone. Bone tissue and blood vessels gradually spread into the coral graft. Eventually, bone replaces most of the coral implant. (viii) The coral reef provides a living laboratory. Both students and scientists can study the interrelationships of organisms and their environment. Those very important coral reefs suffered sharp decline due to several reasons which are both natural and anthropogenic. So, urgent strategies are needed to save coral reefs, the most important of which is coral

B I O D I V E R S IT A S 14 (1): 43-53, April 2013

transplantation. The purpose of the present work is to provide a review for current trends in coral transplantation as a basis for preserving biodiversity.

(2009) developed a coastal environmental assessment system using coral recruitment. No coral conservation strategy will be effective until underlying intrinsic and/or extrinsic factors driving high mortality rates are understood and mitigated or eliminated (Garrison and Ward 2012).

NEED FOR CORAL CONSERVATION The increasing rates of coral mortality associated with the rise in stress factors and the lack of adequate recovery worldwide have urged recent calls for actions by the scientific, conservation, and reef management communities (Rinkevich 2008; Teplitski and Ritchie 2009). In cases of acute physical damage to reefs, such as in ship groundings, sophisticated engineering methods have been developed to mitigate damage and to maximize recovery and are used in combination with substrate stabilization and colony transplantation (e.g. Jaap et al. 2006). Loss of live coral cover has been more related to abnormally high sea-surface temperatures and incidence of diseases, rather than direct human activities (e.g. Miller et al. 2009). De Vantier et al. (2006) studied the indicators of management effectiveness in Bunaken National Park. On a global scale, the value of total economic goods and services provided by coral reefs have been estimated to be US$375 billion per year with most of this coming from recreation, sea defense services and food production, that equates to an average value of around US$6,075 per hectare of coral reefs per year (Edwards and Gomez 2007). Degradation of reefs means the loss of these economic goods and services, and loss of food security to people living in coastal areas (Sutton and Bushnell 2007). Reef restoration may face economic, legal, social and political constraints which are very much critical to coral reef conservation policies like the ecological factors (Job et al. 2003). Recently, restoration strategies have focused on the broader conservation effort, emphasizing the need to combine local management actions, such as establishment of no-harvest marine reserves and effective management of the coastal zone (both terrestrial and marine), with direct actions, such as transplantation (Mumby and Steneck 2008, Bruckner et al. 2009). Transplantation of coral colonies or fragments, whether from aqua-, mariculture or harvesting from a healthy colony, has been the most frequently recommended action for increasing coral abundance on damaged or degraded reefs and for conserving listed or “atrisk” species (Teplitski and Ritchie 2009, Williams and Miller 2010). It has been suggested that newly developed molecular tools be used to optimize selection of coral propagules for cultivation and transplantation, to deepen our understanding of transplant survival (Baums 2008), and to identify and maximize the genetic diversity of transplants (Ammar et al. 2000; Shearer et al. 2009), which is considered essential. Debate continues over the effectiveness of transplantation in conserving threatened coral species, increasing coral abundance, and accelerating reef restoration or enhancement at ecologically relevant temporal and spatial scales. This controversy is due in part to the small scale of transplant studies compared to the scale of reef damage (e.g. Edwards and Gomez 2007) and the relatively short duration of most studies. Roeroe et al.

REHABILITATION VS. RESTORATION Rehabilitation can be defined as ‘‘the act of partially or, more rarely, fully replacing structural or functional characteristics of an ecosystem that have been reduced or lost’’ (Precht 2006). It may also be the substitution of alternative qualities or characteristics than those originally present provided that they have more social, economic or ecological value than existed in the disturbed or degraded state (Elliott et al. 2007) Thus, the rehabilitated state is not expected to be the same as the original state or as healthy but merely an improvement on the degraded state (Bradshaw 2002). Ecosystem restoration has been defined by Baird (2005) as ‘activities designed to restore an ecosystem to an improved condition. However, this does not imply the highest quality of the final ecosystem but merely that it is better than the degraded situation. Because of this, a preferable definition of restoration is ‘the process of re-establishing, following degradation by human activities, a sustainable habitat or ecosystem with a natural (healthy) structure and functioning’ (Livingston 2006, Yeemin et al. 2006). Simenstad et al. (2006) and Van Cleve (2006) take this to be returning an ecosystem to its predisturbance condition and functioning.

TRANSPLANTATION OF STORM-GENERATED CORAL FRAGMENTS Transplantation of coral colonies or fragments, whether from aqua-, mariculture or harvesting from a healthy colony, has been the most frequently recommended action for increasing coral abundance on damaged or degraded reefs and for conserving listed or “at-risk” species (Ammar et al. 2000; Rojas et al. 2008; Teplitski and Ritchie 2009; Shaish et al. 2010). Yet there is a deepening awareness that no habitat, once damaged or degraded, can be restored to its original condition and that the basic factors causing declines must be addressed if restoration of reefs and conservation of threatened reef species are to succeed over time (Bruno and Selig 2007). In response to dramatic losses of reef-building corals and ongoing lack of recovery, a small-scale coral transplant project was initiated in the Caribbean (U.S. Virgin Islands) in 1999 and was followed for 12 years (Garrison and Ward 2012). The primary objectives were to (i) identify a source of coral colonies for transplantation that would not result in damage to reefs, (ii) test the feasibility of transplanting storm-generated coral fragments, and (iii) develop a simple, inexpensive method for transplanting fragments that could be conducted by the local community. The ultimate goal was to enhance abundance of threatened reef-building species on local reefs. Storm-produced coral fragments of two threatened

AMMAR et al. â&#x20AC;&#x201C; Current trends in coral transplantation

reef-building species [Acropora palmata and A. cervicornis (Acroporidae)] and another fast-growing species [Porites porites (Poritidae)] were collected from environments hostile to coral fragment survival and transplanted to degraded reefs. Inert nylon cable ties were used to attach transplanted coral fragments to dead coral substrate. Survival of 75 reference colonies and 60 transplants was assessed over 12 years. Only 9% of colonies were alive after 12 years: no A. cervicornis; 3% of A. palmata transplants and 18% of reference colonies; and 13% of P. porites transplants and 7% of reference colonies. Mortality rates for all species were high and were similar for transplant and reference colonies. Physical dislodgement resulted in the loss of 56% of colonies, whereas 35% died in place. Only A. palmata showed a difference between transplant and reference colony survival and that was in the first year only. Location was a factor in survival only for A. palmata reference colonies and after year 10. Even though the tested methods and concepts were proven effective in the field over the 12-year study, they do not present a solution. No coral conservation strategy will be effective until underlying intrinsic and/or extrinsic factors driving high mortality rates are understood and mitigated or eliminated.

SAVING LARGE CORALS DURING THE CONSTRUCTION OF A LIQUIFIED NATURAL GAS PLANT As parts of a mitigation measure associated with the construction of a Liquefied Natural Gas plant, four large coral transplantations were carried out in Yemen between January and October 2007 (Seguin et al. 2008). Around 1,500 selected coral colonies were removed from areas to be impacted, transported and cemented in new sites. Transplanted colonies belong to 36 species and 25 genera. Among these, 140 large Porites spp. weighing from 200 kg up to 4 tonnes, were moved using new transplantation techniques. Growth, in situ mortality and health of the transplants were monitored over one year using photo quadrates, close-up pictures and linear growth measurements. Overall, survival of corals one year after transplantation was 91%. Most losses of transplants were apparently due to sedimentation of fine particles in the transplanted areas, fish predation, fisher activity and swell effects. Evidence of coral growth after transplantation was observed, especially in Acropora and Porites species, and on some faviids. The transplantation results demonstrate the capacity of corals to adapt to a new environment, in favorable conditions. They show that carefully designed coral reef rehabilitation strategies can be part of industrial development processes, whenever necessary.

TRANSPLANTATION OF JUVENILE CORALS Clark and Edwards (1994) suggested that transplantation of mature coral colonies may help restore degraded reefs. However, such procedures cause damage to

other reef areas and are labor intensive. Knowledge obtained on the reproductive patterns and settling preferences of the Red Sea corals (Benayahu et al. 1990) urged scientists to assess for the first time the potential use of their propagules for transplantation to an artificial reef. In addition, the unique autotomy process in Dendronephthya hemprichi (Dahan and Benayahu 1997) facilitated the use of its fragments for this purpose. The survivorship rates of transplanted species are related to the structural features of the modular experimental artificial reef (Ammar and Mahmoud 2005).

MASSIVE VS BRANCHING CORALS Branching morphologies are usually used in experiments on coral regeneration for two main reasons: they have a life history with high asexual reproduction by fragmentation (Bruno 1998), and have rapid growth and regeneration (Karlson and Hurd 1993). They are also more fragile than other morphologies, often suffering the most damage from different stresses. The vertical arborescent structure of branching Porites palmata was expected to be snagged, dislodged or damaged by seine net fishing to a greater extent than the spherical or horizontal encrusting structure of P. lutea. Porites palmata is more susceptible to fish predation than the massive species. Massive corals are thus recommended for transplantation due to their low damage and mortality and may ultimately produce the habitat required for fish and other coral morphologies.

SEXUAL REPRODUCTION IN TRANSPLANTED CORAL FRAGMENTS Studies on survivorship and the reproductive ability of transplanted coral fragments are important for coral reef restoration (Forsman et al. 2006). It is especially important to determine the ideal collection time and minimum fragment size that are necessary for successful propagation (Kai and Sakai 2008). This is because the maximum survival rate with the possibility of spawning needs to be established in order to develop successful restoration techniques. For example, aquariums try to establish coral breeding facilities and nurseries using sexually reproducing corals. Although several reports have stated that naturally or artificially occurring fragments reduce fecundity or stop gonad development, those studies were performed only once or just a few times after fragmentation (e.g. Zakai et al. 2000, Okubo et al. 2007). Survivorship and growth of transplanted fragments have been surveyed and discussed (e.g. Yap 2004), but the spawning of fragments had never previously been reported. Connell (1973) postulated that the occurrence of sexual reproduction in a colony is determined by the size of the colony or age of the polyps comprising the colony. Okubo et al. (2009) concluded that transplantation of larger fragments during the cooler season resulted in an increased survival rate and spawning ratio in the 1st year after transplantation in A. nasuta.

B I O D I V E R S IT A S 14 (1): 43-53, April 2013

Figure 1. Use of asexual recruits and molecular biological tools for transplantation studies (Ammar et al. 2000).

Figure 2. Big transplanted branches of Acropora (Photoâ&#x20AC;&#x2122;s copyright: Czaldy Garrote)

AMMAR et al. â&#x20AC;&#x201C; Current trends in coral transplantation

TRANSPLANTATION OF CORALS USING SEXUAL REPRODUCTION AND CERAMIC CORAL SETTLEMENT DEVICE (CSD) A new type of coral-restoration technology has been developed since 1999 (Peterson et al. 2005, Okamoto et al. 2005, 2008, 2010) to overcome bleaching and degradation caused by global warming (Carpenter et al. 2008; Okamoto et al. 2007; Sato 2008). A case study was done by Okamoto et al. (2012) who conducted a survey of the coral community structure and recruitment of Acropora in six sites around Manado, Indonesia, in 2007 and 2008. They found that the population of Acropora corals as well as recruitment of juvenile coral was extremely low. To examine the future of Acropora corals around Manado, they assessed the reproduction potential of Acropora at two sites of Bunaken Island. As a result, spawning was estimated to occur several times in 2007. Anyway, Isopora corals could not be separated from Acropora (hereafter referred to as Acroporidae). The number of Acroporidae that settled on Coral Settlement Devices (CSDs) and Marine Block (MB) plates was very low. The spawning peaks of Acropora were estimated to be between February and June, and around October. The spawning around October was lower than that observed between February and June. They attempted to apply a coral restoration method using sexual reproduction developed and successfully applied in Japanâ&#x20AC;&#x2122;s largest coral reef, Sekisei Lagoon, to prevent the extinction of Acropora. For the experiments, they used CSDs to settle and raise corals in situ for transplantation and MB plates as artificial substratum on sandy bottom areas. The ceramic coral settlement device (CSD) contained within a polypropylene case is fixed to the sea bottom 1 week before mass spawning. Settled corals were raised in situ for approximately one and half year (corals grew to approximately 1.5 cm in diameter). These corals were transplanted to coral reefs or onto marine blocks (MBs) on a sandy bottom. CSDs have been improved by applying the results of in situ examination with regard to materials, shapes, and arrangement within a case. A small CSD case makes the following features easy: underwater handling, deployment at the settlement site, and transportation to the nursery and restoration site. The CSD case is readily transportable between the sea and the water tank onboard a ship in a small plastic bucket filled with seawater.

INCREASING SUBSTRATE FOR SETTLEMENT On a damaged reef, the availability of suitable substrate for larval settlement can rapidly decrease due to algal or soft coral overgrowth, and sedimentation (Schlacher et al. 2007). Minimizing land based sources of nutrient enrichment and maintaining algae-eating fish populations will help reduce algae. Techniques for actively increasing suitable substrate are briefly described below. Introducing artificial surfaces for larval settlement Artificial reefs such as concrete blocks, wrecks or other purpose-designed structures may have an additional benefit

for fisheries management but the cost may be prohibitive for large areas. Encouraging natural surfaces This can be done by stabilizing or removing loose substrate material (such as coral fragments) and removing algae and other organisms that might inhibit larval settlement or damage young recruits. Certain substrates, e.g. Goniastrea skeletons, appear to induce settlement and larval metamorphosis. This approach should only be taken if expert scientific advice is available. Creating new surfaces through electrolysis A unique technology developed by a German architect named Wolfe H. Hilbertz in 1977 involves precipitation of ionic calcium and magnesium in seawater to form a carbonate substrate under the presence of low direct current underwater (Hilbertz 1992). This substrate may serve as a natural platform for the transplanted corals and subsequent colonization of marine larvae (Ammar 2001; Schillak et al. 2001). The three hypotheses concerning growth enhancement mechanisms suggested by Hilbertz and Goreau (1996) are not fully explored experimentally. The first hypothesis is that the electric field that enables accretion may cause the precipitated carbonates to attach directly to the skeletons of coral transplants. The second is that the method induces CaCO3 enrichment of water in the immediate vicinity of the coral, thereby enhancing natural calcification. The third one is that excess production and release of electrons due to the electrochemical processes occurring within the vicinity of the coral might affect the electron-transport chain for ATP production where the excess energy can be used for growth enhancement. This requires considerable financial and human investment, and a source of permanent electrical current while the structure is being built. The long-term impact of the electrical current on marine life is not known. Sabater and Yap (2002) investigated experimentally the effect of electrochemical deposition of CaCO3 on linear and girth growth, survival and skeletal structure of Porites cylindrica Dana. Transplanted coral nubbins were subjected to up to 18 V and 4.16 A of direct current underwater to induce the precipitation of dissolved minerals. Naturally growing colonies showed a significant increase in percentage of longitudinal growth over the treated and untreated corals. Survival followed a similar trend as the growth rate. Lowest survival rates were found in the untreated nubbins. Phenotypic alterations were observed in the treated nubbins where the basal corallites decreased in size with a concomitant increase in their number per unit area. This was probably due to increased mineral concentration (such as Ca2+ , Na-, Mg2+ , CO32-, Cl-, OH-, and HCO3-) at the basal region of the nubbins. These alterations were accompanied by a significant increase in girth growth rates of the treated nubbins at their basal regions. The abundance of mineral ions at the basal region thus appeared to be utilized by the numerous small polyps for a lateral increase in size of the nubbins instead of a longitudinal increase.

B I O D I V E R S IT A S 14 (1): 43-53, April 2013

CHEMICAL SIGNALS AND SURFACE CHEMISTRY The topics of surface chemistry (Spieler et al. 2001) and the possible inputs of toxic leachate from artificial substrates were discussed and considered as important factors for enhancing natural recruitment (Ammar 2009). At least one artificial reef manufacturer (Reef Ball) recommended the addition of microsilica to concrete to provide a neutral pH surface. In addition, the organic and microbial biofilm that is quickly formed on any clear substrate that is immersed in seawater may provide negative settling cues. It is also well documented that initial colonizing microbial algal and invertebrate assemblages may affect settlement of coral larvae; moreover the chemical glycosaminoglycan isolated from a coralline alga (Hydrolithon boergesenii) that signals Agaricia agaricites humilis larvae to settle, the synthesized material, called â&#x20AC;&#x153;coral flypa perâ&#x20AC;?, proved effective for attracting larvae (Rinkevich 2005).

the presence of algae was compared with that of corals in cleared plots, transplants in the latter instances survived better (Soong and Chen 2003). Invertebrate corallivores Cros and McClanahan (2003) found the coral-eating snail Drupella cornus on one block of transplants preying on Porites palmata in the vicinity of a large patch of dead Acropora. There were three to four snails on each branching coral and they killed 60% of each colony/transplant, mostly at the base. This was similar to previous observations of D. cornus preying on the genus Acropora and the family Pocilloporidae on damaged reefs in Kenya and Western Australia (Turner 1994). In the past, damage by Drupella outbreaks has been compared to damage by crown-of-thorns (COTs) outbreaks (Cumming 1999). Reports of mass mortality due to this snail have been recorded in Western Australia and Japan (Turner 1994). Outbreaks have been in part attributed to over fishing and the removal of key predators of the snail (McClanahan 1994).

THREATS TO CORAL TRANSPLANTATION Coral algal transition in coral transplantation experiments Yap et al. (2011) found that coral transplantation experiments can provide a useful platform by which to examine the overgrowth of coral by algae under different environmental conditions. Macroalgae are well known competitors of corals for space and light (Lirman 2001, Diaz-Pulido 2009). They can cause damage to coral tissue, or the demise of coral colonies. However, the debate continues as to whether the algae themselves are capable of outcompeting, and then overgrowing, healthy coral colonies. It is believed that algal spores or filaments generally do not settle directly on live corals (McCook 2001). However, when established algae come in direct contact with corals on the reef, this can cause shading, tissue abrasion, and/or overgrowth (Quan-Young and Espinoza-Avalos 2006). Abrasive contact or overgrowth can eventually result in partial or total coral mortality. Live corals are also capable of overgrowing algae (Diaz-Pulido et al. 2009) and inhibiting algal growth (Nugues et al. 2004). Once established, algal populations tend to persist, thus hindering reestablishment of coral populations via recruitment (Kuffner et al. 2006) or the regrowth of adult colonies. Algal overgrowth is one major problem (Shaish et al. 2010). It can be a significant factor that hampers the success of coral restoration efforts because of reduced growth or mortality of the transplants. Under certain conditions, coral transplants appear unable to resist algal invasion, and eventually die, apparently because of smothering (Dizon and Yap 2006). In some cases, algae were observed to cause bleaching of the underlying coral tissue (Rojas et al. 2008). The bleached tissue subsequently deteriorated. Contact with algae can cause direct stress to coral tissue, after which the algae proceed to overgrow the coral (Quan-Young and Espinoza-Avalos 2006). In experiments where the performance of coral transplants in

ROLE OF AUTUTROPHS FOR TRANSPLANTED CORALS Primary producers, or autotrophs, make up the base of all food chains, however, they are capable of synthesizing complex organic compounds such as glucose from a combination of simple inorganic molecules and light energy in a process known as photosynthesis (Baum et al. 2003). The same author further indicated that some common autotrophs in a coral reef ecosystem are phytoplankton, coralline algae, filamentous turf algae, the symbiotic zooxanthellae in corals, and many species of seaweed. Phytoplanktons are one of the most important primary producers in the world and include a wide variety of organisms. Those organisms include: 1-diatoms which are the most productive type of phytoplankton 2dinoflagellates and silicoflagellates which move by way of flagella 3-coccolithophores which have peels made of calcium carbonate 4-cyanobacteria, and other extremely small phytoplankton species referred to as nanoplankton (2.0-20 mm) and 5-picoplankton (0.2-2.0 mm). In brief, the phytoplanktons are important for providing transplanted corals with complex organic compounds through photosynthesis.

REGENERATION AND GROWTH OF CORAL FRAGMENTS IN A NURSERY Soong and Chen (2003) indicated that one of the effective and commonly used methods to restore coral communities is the transplantation of coral colonies or fragments. The same author, in this investigation, used fragments of Acropora in a semiprotected nursery in southern Taiwan between 1996 and 1998. The possible effects of different factors on the generation of new branches and the initial skeletal extension rates of

AMMAR et al. – Current trends in coral transplantation

transplants were tested. The variables under study were the origin and length of the fragments, their new orientation, presence of tissue injury, and position in the fragment. All these factors were found to make a difference in either one or both aspects of coral growth (i.e., branching frequency and skeletal extension rate). These two factors clearly determine the success rate of a small fragment developing into a large colony that has a much higher probability to survive and grow on its own. It was found the success of coral fragments in a semiprotected nursery depended on many factors. With all factors taken into consideration, a large amount of acroporid corals could be produced within a reasonable period. These materials can then be used either to restore natural populations directly or to satisfy the market demand for live corals, which would obviously reduce exploitation of natural populations. Branching acroporids are known to translocate nutrients directionally, which leads to faster extension rates of axial polyps (Fang et al. 1989). Likewise, the ability of corals to regenerate was found to be dependent on the position of the injuries in the colonies. In Acropora palmate the regenerative capability decreases away from the growing edge (Meesters and Bak 1995). In a multispecies comparison, however, no position effect was found in the regenerative ability in six of seven species (Hall 1997). The results of orientation experiments on fragments without axial polyps, however, indicate that the distal or proximal ends in the original colony did not have any inherent advantage in generating new axial polyps. Instead, the local environment determined the end at which new axial polyps were produced. It is possible that all the branches we used in the experiment were distal branches of the colonies and that the two ends of the 6-cm fragments posed little difference in ontogenic gradients along the branches. Accordingly, whichever end pointed upward had a higher frequency of generating new axial polyps. It may be concluded that the resulting new branches are likely to be distributed in the upper portions of fragments. This characteristic is potentially adaptive in that branches in lower shaded regions of a colony tend to be overgrown and smothered by other organisms or sediments (Meesters et al. 1997). Coral fragments are transplanted to a protected site and ‘grown out’ to a certain size before being used for rehabilitation and for creating new fragments. The source of fragments must be chosen with care, to avoid damage to other reefs. Coral farms potentially have an additional benefit as an attraction for snorkelers. Further investigation is required to reduce costs and increase success rates. The concept of nursery installed on the sea floor has already been applied to corals (Rinkevich 2005). One of the major ex situ restoration approaches is the collection, settlement, and maintenance of planula larvae and spats under optimal conditions (Epstein et al. 2003). The in situ nursery approach sustains the mariculture of nubbins, coral fragments, and small colonies. A coral nursery may also be considered as a pool for local species that supplies reefmanagers with unlimited coral colonies for sustainable management (Epstein et al. 2003). Both ex situ and in situ approaches can also provide ample material for the coral

trade, thus reducing collections of coral colonies from the wild (Heeger and Sotto 2007).

BIOGEOCHEMICAL PROCESSES AND NUTRIENT CYCLING WITHIN AN ARTIFICIAL REEF Reef structures, by providing protection for marine species, can result in marine system biomass enhancement (Godoy et al. 2002). As a result of biomass enhancement, sediment becomes more active in the process of nutrient regeneration providing a nutritional source for other forms within the ecosystem, or being exported by water movements increasing the general productivity of neighbouring areas, furthermore, planktivorous fish species can induce nutrient production in the water column, excreting substantial amounts of ammonium, urea and depositing organic material, which is then incorporated into the reef food web (Falcao et al. 2006).

SUCCESSFUL CORAL TRANSPLANTATION For a successful coral transplantation, selection of proper area to be used for transplantation is necessary (Okubo et al. 2005). It has been mentioned that the transplantation might not be suitable in an area where the coral recruitment has failed over the years. This is because the transplanted corals may not recruit. Also studies have shown signiﬁcant effects of environmental factors (eg. light, temperature, sedimentation and water movement) on growth and/or survival of coral transplants (Montebon and Yap 1995; Palomar et al. 2009). Choice of a particular habitat for coral transplantation is therefore a critical aspect of coral transplantation studies. One more problem in coral transplantation is the selection of species to be transplanted. Studies have shown that different coral species show different growth and survival after transplantation due to the differences in their life history strategies (Yap et al. 1992). Till now only selected species have been used in the transplantation studies. But information on the suitability of a particular coral species for transplantation and their responses to relocation needs to be established by more research. Edwards and Clark (1998) have argued that there has been too much focus on transplanting fast growing branching corals over slow growing massive corals. They further mention that fast growing branching corals although recruit fast, are not able to survive the effect of transplantation and relocation. Another factor to be considered in the coral transplantation efforts is the size of coral colonies or fragments. In the previous studies, it has been shown that the size of the coral plays an important role in the survival of transplanted fragments (Bowden-Kerby 1996, 2009). However, the relationship between colony size and growth was shown to be signiﬁcant for some species, but not in others (Clark and Edwards 1995). Miyazaki et al. (2010) observed the survival and growth of transplanted fragments of the reef coral species Acropora hyacinthus and Acropora muricata over a period of 3 years from

B I O D I V E R S IT A S 14 (1): 43-53, April 2013

Figure 3. Coral farming (Rinkevich 2005)

B C Figure 4. A new innovated and cheap model for building artificial reefs (Ammar and Mahmoud 2005). (A) New buds at the top of the branch. (B) A thick layer of the substrate built after 9 months of installing the unit. (C) Algae settling on the built substrate.

AMMAR et al. â&#x20AC;&#x201C; Current trends in coral transplantation

November 1999 to November 2002 in a high-latitude coral community in Shirigai National Marine Park, Otsuki, Kochi Prefecture, Japan. A total of 36 coral fragments (a total area of 4.4 m2) (thirty one A. hyacinthus fragments and five A. muricata fragments) were transplanted into 3 separate blocks at 3-4 m depth with each block consisting of approximately equal number of coral fragments in each species. Out of 36 coral fragments transplanted, all A. muricata fragments died before the first survey (one year after the transplantation) and only 29 A. hyacinthus fragments survived the initial relocation. The results showed an increase in the coral cover to 48% of the total area form the initial 8.9% in case of A. hyacinthus. There was a horizontal increase in the coral size resulting in the accretion of the coral skeleton with the neighboring coral fragments. Transplanted fragments grew rapidly (6.9-15.8 cm) in the warmer (17-25ÂşC) months compared to the slower growth (0.9-4.8 cm) in the colder (below 17ÂşC) months.

CONCLUSION Coral transplantation should be carried out by people with relevant experience. Prior to considering coral transplantation, ensure that the transplant site is not subject to ongoing impacting processes, such as strong waves, shallow water snorkel areas, crown-of-thorns (COTs) infestation, or shading by structures or vessels. Ensure donor areas have a sufficient healthy and diverse coral cover. Total coral collection impacts must be within the natural variability of the area and must not significantly reduce the donor area coral cover or species composition. For the transplant site, identify and record the proposed species, numbers, sizes and placement of the individual colonies to be transplanted. Document a methodology, addressing careful removal, fragmentation, handling and attachment of corals, and describing how impacts to live tissue will be minimized. Transplant all corals to the same depth, aspect, habitat, water flow, proximity to adjacent colonies and orientation as the site from which they were removed. Consider interactive impacts between adjacent colonies. Tag, photograph and otherwise easily and accurately identify each transplanted colony for the duration of the transplantation and at least 12 months following completion of the project. Carefully maintain the transplants. Revisit and reattach corals at least weekly in the first month and at least fortnightly in the next three months. A coral nursery may be considered as a pool for local species that supplies reef-managers with unlimited coral colonies for sustainable management. Recoverability depends on the stressor, the impacted species/community and the temporal and spatial intensities of the stressor. the larger the transplanted fragment, the greater the probability of survival (Garrison and Ward 2012). Transplanting corals for making artificial reefs can be useful in increasing biodiversity; providing tourist diving, fishing and surfing; creating new artisanal and commercial fishing opportunities; colonizing structures by fishes and invertebrates). Artificial

reefs can have a positive economic impact which is significant and may reach several hundreds of million dollars per year. Coral transplantation will not be effective in conserving coral species or in assisting reef recovery over time until the underlying factors causing degradation of reefs and mortality of corals are understood, addressed, and eliminated or mitigated.

REFERENCES Ammar MSA. 2001. Improvement of the molecular and physiological behavior of the reef coral Stylophora pistillata at Hurghada, Red Sea, Egypt by using the ARCON substrate. J Egyp Acad Soc Environ Develop 2: 205-219. Ammar MSA. 2009. Coral reef restoration and artificial reef management, future and economic. Open Environ Eng J 2: 37-49. Ammar MSA, Mahmoud MA. 2005. A new innovated and cheep model in building artificial reefs. Egyp J Aq Res 31: 105-118. . Ammar MSA, Amin EM, Gundacker D, Mueller WEG. 2000. One rational strategy for restoration of coral reefs: application of molecular biological tools to select sites for rehabilitation by asexual recruits. Mar Pollut Bull 40: 618-627. Baird RC. 2005. On sustainability, estuaries and ecosystem restoration: the art of the practical. Rest Ecol 13: 154-158. Baum JK, Myers RA, Kehler DG, Wor, Harley J, Doherty PA. 2003. Collapse and conservation of shark populations in the Northwest Atlantic. Science 299: 389-392. Baums IB. 2008. A restoration genetics guide for coral reef conservation. Mol Ecol 17: 2796-2811. Benayahu Y, Weil D, Kleinman M. 1990. Radiation of broadcasting and brooding patterns in coral reef alcyonaceans. In: Hoshi M, Yamashita O (eds) Advances in invertebrate reproduction 5. Elsevier, New York. Bowden-Kerby A. 1996. Coral transplantation in sheltered habitats using unattached fragments and cultured colonies. Proc. 8th Int. Coral Reef Symp. Panama. Bowden-Kerby A. 2009. Restoration of threatened Acropora cervicornis corals: intraspecific variation as a factor in mortality, growth, and self-attachment. Proc. 11th Int. Coral Reef Symp., Ft. Lauderdale, Florida 2: 1194-1198. Bradshaw AD. 2002. Introduction and philosophy. In: Perrow MR, Davy AJ (eds.). Handbook of Ecological Restoration: Principles of Restoration. Cambridge University Press, Cambridge. Bruckner AW, Bruckner RJ, Hill R. 2009. Improving restoration approaches for Acropora palmata: Lessons from the Fortuna Reefer grounding in Puerto Rico. Proc. of the 11th Int. Coral Reef Symp. Ft. Lauderdale, Florida 2: 1199-1203. Bruno JF. 1998. Fragmentation in Madracis mirabilis (Duchassaing and Michelotti): how common is size-specific fragment survivorship in corals? J Exp Mar Biol Ecol 230: 169-181. Bruno JF, Selig ER. 2007. Regional decline of coral cover in the IndoPacific: Timing, extent, and subregional comparisons. PLos ONE 8: e711. Carpenter KE et al. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impact. Science 321: 560-563 Clark S, Edwards AJ. 1994. Use of artificial reef structures to rehabilitate reef degraded by coral mining in the Maldives. Bull Mar Sci 55 (2-3): 724-744. Cros A, McClanahan T. 2003. Coral transplant damage under various management conditions in the Mombasa Marine National Park, Kenya. Western Indian Ocean. J Mar Sci 2 (2): 127-136. Cumming RL. 1999. Predation on reef-building corals: multiscale variation in the density of three corallivorous gastropods, Drupella spp. Coral Reefs 18: 147-157. Dahan M, Benayahu Y. 1997. Reproduction of Dendronephthya hemprichi (Cnidaria: Octocorallia) : year-round spawning in an azooxanthellate soft coral. Mar Biol 129: 573-579. DeVantier L, Turec M, Skelton P. 2006. Ecological assessment of the coral communities of Bunaken Natuonal Park: Indicators of management effectiveness. Proc 10th ICRS, Okinawa.

B I O D I V E R S IT A S 14 (1): 43-53, April 2013

Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans, RD, Williamson DH, HoeghGuldberg O. 2009. Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS ONE. 4: e5239. Dizon, RM Yap HT. 2006. Effects of multiple perturbations on the survivorship of fragments of three coral species. Mar Pollut Bull 52: 928-934. Edwards AJ, Clark S. 1998. Coral transplantation: a useful management tool or misguided meddling? Mar Poll Bull 37: 474-487. Edwards AJ, Gomez ED. 2007. Reef restoration concepts and guidelines: Making sensible management choices in the face of uncertainty. Coral Reef Targeted Research and Capacity Building for Management Programme, St. Lucia and Australia 4: 1-38. Elliott M, Burdon D, Hemingway KL, Apitz SE, Estuarine SE. 2007. Coastal and marine ecosystem restoration: confusing management and science-A revision of concepts, Estuarine. Coast Sh Sci 74: 349366. Epstein N, Bak RPM, Rinkevich B. 2003. Applying forest restoration principles to coral reef rehabilitation. Aq Conserv 13: 387-395. Falcao M, Santos MN, Vicente M., Monteiro CC. 2006. Biogeochemical processes and nutrient cycling within an artificial reef off Southern Portugal. Mar Environ Res 63: 429-444. Fang, LS, Chen YWJ, Chen CS. 1989. Why does the white tip of stony coral grow so fast without zooxanthellae? Mar Biol 103: 359-363. Forsman ZH, Rinkevich B, Hunter CL. 2006. Investigating fragment size for culturing reef-building corals (Porites lobata and P. compressa) in ex situ nurseries. Aquaculture 261: 89-97. Garrison VH, Ward G. 2012. Transplantation of storm-generated coral fragments to enhance Caribbean coral reefs: A successful method but not a solution. Rev Biol Trop 60 (Suppl. 1): 59-70. Godoy EAS, Almeida TCM, Zalmon IR. 2002. Fish assemblages and environmental variables on an artificial reef north of Rio de Janeiro, Brazil. ICES J Mar Sci 59: 138-143. Great Barrier Reef Marine Park Authority (GBRMPA). Coral transplantation at tourism sites. Permit Information Bulletin. permitenquiry@gbrmpa.gov.au Hall VR. 1997. Interspecific differences in the regeneration of artificial injuries on scleractinian corals. J Exp Mar Biol Ecol 212: 9-23. Heeger T, Sotto F (eds). 2007. in Coral Farming: A Tool for Reef Rehabilitation and Community Ecotourism. German Ministry of Environment (BMU), German Technical Cooperation and Tropical Ecology Program (GTZ-TÖB), Philippines. Hilbertz WH. 1992. Solar generated building material from seawater as a sink for carbon. Ambio 21: 126-129. Hilbertz WH, Goreau TJ. 1996. A method for enhancing the growth of aquatic organisms and structure created. thereby. http: //www.uspto.gov, US Patent #08/374993. Jaap WC, Hudson JH, Dodge RE, Gilliam D, Shaul R. 2006. Coral reef restoration with case studies from Florida: p. 478-514. In: Côte M, Reynolds D (eds.). Coral Reef Conserv. Univ. Cambridge Press, Cambridge, UK. Job S, Schrimm M, Morancy R. 2003. Reef Restoration: Practical guide for management and decision-making. Carex Environnment, Ministère de l’Écologie et du Dévelopement Durable, IFRECOR. Kai S, Sakai K. 2008. Effect of colony size and age on resource allocation between growth and reproduction in the corals Goniastrea aspera and Favites chinensis. Mar Ecol Prog Ser 354: 133-139. Karlson RH, Hurd LR. 1993. Disturbance, coral reef communities, and changing ecological paradigms. Coral Reefs 12: 177-125. Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS. 2006. Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar Ecol Prog Ser 323: 107-117. Lirman D. 2001. Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 19: 392-399. Livingston RJ. 2006. Restoration of Aquatic Ecosystems, Boca Raton, Florida: Taylor and Francis. p. 423. McClanahan TR. 1994. Coral-eating snail Drupella cornus population increases in Kenyan coral reef lagoons. Mar Ecol Prog Ser 115: 131137. McCook LJ. 2001. Competition between corals and algal turfs along a gradient of terrestrial influence in the nearshore central Great Barrier Reef. Coral Reefs 19: 419-425. Meesters EH, Bak RPM. 1995. Age-related deterioration of a physiological function in the branching coral Acropora palmata. Mar Ecol Prog Ser 121: 203-209.

Meesters EH, Wesseling I, Bak RPM. 1997. Coral colony tissue damage in 6 species of reef-building corals—partial mortality in relation with depth and surface-area. J Sea Res 37: 131-144. Miller J, Muller E, Rogers C, Waara R, Atkinson A, Whelan KRT, Patterson M, Witcher B. 2009. Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands. Coral Reefs 28: 925-937. Miyazaki K, Keshavmurthy S, Fukami S. 2010. Survival and growth of transplanted coral fragements in a high-latitude coral community (32° N) in Kochi, Japan. Kuroshio Biosphere 6: 1-9. Montebon ARF, Yap HT. 1995. Metabolic responses of the scleractinian coral Porites cylindrica Dana to water motion. I. Oxygen ﬂux studies. J Exp Mar Biol Ecol 186: 33-52. Mumby PJ, Steneck RS. 2008. Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23: 555-563. Nugues MM, Delvoye L, Bak RPM. 2004. Coral defence against macroalgae: differential effects of mesenterial filaments on the green alga Halimeda opuntia. Mar Ecol Prog Ser 278: 103-114. Okamoto M, Nojima S, Fujiwara S, Furushima Y. 2008. Development of ceramic settlement devices for c coral reef restoration using in situ sexual reproduction of corals. Fish Sci. 74: 1245-1253. Okamoto M, Nojima S, Furushima Y, Phoel WC. 2005. A basic experimental of coral culture using sexual reproduction in the open sea. Fish Sci 71: 263-270. Okamoto M, Roeroe KA, Yap M, Lalamentic LT, Fujiwara S, Oyamada K. 2012. Experimental transplantation of corals using sexual reproduction in Manado, Indonesia. Proc. 12th Int. Coral Reef Symp., Cairns, Australia, 9-13 July (2012). 20A Restoration of coral reefs. Okamoto M, Yap M, Roeroe KA, Nojima S, Oyamada K, Fujiwara S, Iwata I. 2010. In situ growth and mortality of juvenile Acropora over two years following mass spawning in Sekisei Lagoon, Okinawa. Fish Sci 76: 343-353. Okamoto M., Nojima S, Furushima. 2007. Temperature environments during coral bleaching events in Sekisei Lagoon. Bull Jpn Soc Fish Oceanogr 71: 112-121. Okubo N, Motokawa T, Omori. 2007. When fragmented coral spawn? Effect of size and timing on survivorship and fecundity of fragmentation in Acropora formosa. Mar Biol 151: 353-363. Okubo N, Taniguchi H, Omori M. 2009. Sexual Reproduction in Transplanted Coral Fragments of Acropora nasuta. Zoolog Stud 48 (4): 442-447. Okubo N, Taniguchi H, Motokawa T. 2005. Successful methods for transplanting fragments of Acropora formosa and Acropora hyacinthus. Coral Reefs 24: 333-342. Palomar MJS, Yap HT, Gomez, ED. 2009. Coral transplant survival over 3 years under different environmental conditions at the Hundred Islands, Philippines. Philipp Agric Sci 92: 143-152. Petersen D, Hatta M, Laterveer M, van Bergen D. 2005. Ex situ transportation of coral larvae for research, conservation, and aquaculture. Coral Reefs 24: 510-513. Precht WF (ed). 2006. Coral Reef Restoration Handbook. CRC Press, Boca Raton. Quan-Young LI, Espinoza-Avalos J. 2006. Reduction of zooxanthellae density, chlorophyll a concentration, and tissue thickness of the coral Montastrea faveolata (Scleractinia) when competing with mixed turf algae. Limnol Oceanogr 51: 1159-1166. Rinkevich B. 2005. The coral gardening concept and the use of underwater nurseries: lessons learned from silvics and silviculture. In: Coral Reef Restoration Handbooks, The Rehabilitation of an Ecosystem Under Siege; Precht WE Ed. 291-300, Press. Rinkevich B. 2008. Management of coral reefs: We have gone wrong when neglecting active reef restoration. Mar Poll Bull 56: 1821-1824. Roeroe AK, Yap M, Okamoto M. 2009. Development of a coastal environment assessment system using coral recruitment. Fish Sci 75: 214-224. Rojas PT Jr., Raymundo LJ, Myers RL. 2008. Coral transplants as rubble stabilizers: a technique to rehabilitate damaged reefs. In: Proc. 11th Int. Coral Reef Symp. Ft. Lauderdale, Florida. 1262-1266. Sabater MG, Yap HT. 2002. Growth and survival of coral transplants with and without electrochemical deposition of CaCO3. J. Exp. Mar. Biol. Ecol. 272: 131-146. Sato T. 2008. Coral bleaching event on summer 2007. at the Sekisei Lagoon. Lagoon 10: 13-14 [Japanese]. Schillak L, Ammar MSA, Mueller WEG. 2001. Transplantation of coral species to electrochemical produced hard substrata: (Stylophora

AMMAR et al. â&#x20AC;&#x201C; Current trends in coral transplantation pistillata Esper, 1797 and Acropora humilis Dana, 1846), ACP-EU Fish. Res. Report, 2001, 10: 68-84. Mombasa, Kenya, Brussels 19-22 June 2000. Schlacher TA, Stark J and Fischer APB. 2007. Evaluation of artificial light regimes and substrate types for aquaria propagation of the staghorn coral Acropora solitaryensis. Aquaculture 269 (1): 278-289. Seguin F, Le Brun O, Hirst R , Al-Thary I, Dutrieux E. 2008. Large coral transplantation in Bal Haf (Yemen): an opportunity to save corals during the construction of a Liquefied Natural Gas plant using innovative techniques. Proc. 11th Int. Coral Reef Symp. Ft. Lauderdale, Florida. 1267-1270. Shaish L, Levy G, Katzir G, Rinkevich B. 2010. Coral reef restoration (Bolinao, Philippines) in the face of frequent natural catastrophes. Restor Ecol 18: 285-299. Shaish L, Levy G, Katzir G, Rinkevich B. 2010. Coral reef restoration (Bolinao, Philippines) in the face of frequent natural catastrophes. Restor Ecol 18: 285-299. Shearer TL, Porto I, Zubillaga AL. 2009. Restoration of coral populations in light of genetic diversity estimates. Coral Reefs 28: 727-733. Simenstad C, Reed D, Ford M. 2006. When is restoration not? Incorporating landscape-scale processes to restore self-sustaining ecosystems in coastal wetland restoration. Ecol Eng 26: 27-39. Soong K., Chen TA. 2003. Coral transplantation: regeneration and growth of Acropora fragments in a nursery. Restor Ecol 11: 62-71. Spieler RE, Gilliam DS, Sherman RL. 2001. Artificial substrate and coral reef restoration: what do we need to know to know what we need, Bull Mar Sci 69: 1013-1030.

Sutton SG, Bushnell SL. 2007. Socio-economic aspects of artificial reefs: considerations for the great barrier reef marine park. Ocean Coast Manag 50: 829-846. Teplitski M, Ritchie K. 2009. How feasible is the biological control of coral diseases? Trends Ecol Evol 24: 378-385. Turner SJ. 1994. The biology and population outbreaks of the corallivorous gastropod Drupella on Indo-Pacific reefs. Oceanogr Mar Biol Annu Rev 32: 461-530. Van Cleve FB, Leschine T, Klinger T, Simenstad C. 2006. An evaluation of the influence of natural science in regional-scale restoration projects. Environ Manag 37: 367-379. Williams DE, Miller MW. 2010. Stabilization of fragments to enhance asexual recruitment in Acropora palmata, a threatened Caribbean coral. Restor Ecol 18 (S2): 446-451. Yap HT, Alino PM, Gomez ED. 1992. Trends in growth and mortality of three coral species (Anthozoa: Scleractinia), including effects of transplantation. Mar Ecol Prog Ser 83: 91-101. Yap HT, Alvarez-Molina R, Benjamin CS. 2011. Factors promoting coral algal transition in coral transplantation experiments. Phillip Sci Lett 4 (1): 60-69 Yeemin T, Sutthacheep M, Pettongma R. 2006. Coral reef restoration projects in Thailand. Ocean Coast Manage 49: 562-575. Zakai D, Levy O, Chadwick-Furman NE. 2000. Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis. Coral Reefs 19: 185-188.

THIS PAGE INTENTIONALLY LEFT BLANK

GUIDANCE FOR AUTHORS Aims and Scope ”Biodiversitas, Journal of Biological Diversity” or Biodiversitas encourages submission of manuscripts dealing with all biodiversity aspects of plants, animals and microbes at the level of gene, species, and ecosystem. Article types The journal seeks original full-length research papers, reviews, and scientific feedback (short communication) about material previously published. Acceptance The only articles written in English (U.S. English) are accepted for publication. Manuscripts will be reviewed by managing editor, communicating editor and invited peer review according to their disciplines. Authors will generally be notified of acceptance, rejection, or need for revision within 2 to 3 months of receipt. Manuscript is rejected if the content is not in line with the journal scope, dishonest, does not meet the required quality, written in inappropriate format, has incorrect grammar, or ignores correspondence in three months. The primary criteria for publication are scientific quality and biodiversity significance. The accepted papers will be published in a chronological order. This journal periodically publishes in January, April, July, and October. Uncorrection proofs will be sent to the corresponding author by e-mail as .doc or .docx files for checking and correcting of typographical errors. To avoid delay in publication, proofs should be returned in 7 days. A charge The cost of each manuscript is IDR 250,000,- plus postal cost or IDR 150,000,- for SIB members. There is free of charge for non Indonesian author(s), but need to pay postal cost for hardcopy. Reprints Two copies of journal will be supplied to authors; reprint is only available with special request. Additional copies may be purchased by order when sending back the uncorrection proofs by e-mail. Submission The journal only accepts online submission, through e-mail to the managing editor at unsjournals@gmail.com; better to forward to one of the communicating editor for accelerating evaluation.. The manuscript must be accompanied with a cover letter containing the article title, the first name and last name of all the authors, a paragraph describing the claimed novelty of the findings versus current knowledge, and a list of five suggested international reviewers (title, name, postal address, email address). Reviewers must not be subject to a conflict of interest involving the author(s) or manuscript(s). The editor is not obligated to use any reviewer suggested by the author(s). Copyright Submission of a manuscript implies that the submitted work has not been published before (except as part of a thesis or report, or abstract); that it is not under consideration for publication elsewhere; that its publication has been approved by all co-authors. If and when the manuscript is accepted for publication, the author(s) agree to transfer copyright of the accepted manuscript to Biodiversitas. Authors shall no longer be allowed to publish manuscript without permission. For the new invention, authors suggested to manage its patent before publishing in this journal. Open access The journal is committed to free open access that does not charge readers or their institutions for access. Users are entitled to read, download, copy, distribute, print, search, or link to the full texts of the articles, as long as not for commercial purposes. For the new invention, authors are suggested to manage its patent before published. Preparing the Manuscript 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 AsingIndonesia (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 400600 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. Reference to unpublished data and personal communication should not appear in the list but should be cited in the text only (e.g., Rifai MA 2007, personal communication; Setyawan AD 2007, unpublished data). In the reference list, the references should be listed in an alphabetical order. Names of journals should be abbreviated according to the ISSN List of Title Word Abbreviations (www.issn.org/2-22661-LTWA-online.php). APA style in double space is used in the journal reference as follow: Journal: 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

ISSN: 1412-033X E-ISSN: 2085-4722

SPECIES DIVERSTY Species diversity of Selaginella in Mount Lawu, Java, Indonesia AHMAD DWI SETYAWAN, SUTARNO, SUGIYARTO

1-9

ECOSYSTEM DIVERSTY Endophytic fungi associated with Ziziphus species from mountainous area of Oman and new records SAIFELDIN A.F. EL-NAGERABI, ABDULQADIR E. ELSHAFIE, SULEIMAN S. ALKHANJARI Dynamics of fish diversity across an environmental gradient in the Seribu Islands reefs off Jakarta HAWIS H. MADDUPPA, BEGINER SUBHAN, DONDY ARAFAT, ADITYA BRAMANDITO Variability of soil physical indicators imposed by beech and hornbeam individual trees in a local scale YAHYA KOOCH, SEYED MOHSEN HOSSEINI, SEYED MOHAMMAD HOJJATI, ASGHAR FALLAH Species composition of understory vegetation in coal mined land in Central Bengkulu, Indonesia WIRYONO, ARIF BUHA SIAHAAN Proposing local trees diversity for rehabilitation of degraded lowland areas surrounding springs SOEJONO, SUGENG BUDIHARTA, ENDANG ARISOESILANINGSIH REVIEW Review: Current trends in coral transplantation â&#x20AC;&#x201C; an approach to preserve biodiversity MOHAMMED S.A. AMMAR, FAHMY EL-GAMMAL, MOHAMMED NASSAR, AISHA BELAL, WAHID FARAG, GAMAL EL-MESIRY, KHALED EL-HADDAD, ABDELNABY ORABI, ALI ABDELREHEEM, AMGAD SHAABAN

10-16 17-24 25-30

31-36 37-42

43-53

Front cover: Pterois volitans

(PHOTO: ALBERTO ZAFFONATO)

Published semiannually

PRINTED IN INDONESIA ISSN: 1412-033X

E-ISSN: 2085-4722