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BIODIVERSITAS ISSN: 1412-033XVolume 14, Number 1, April 2013 E-ISSN: 2085-4722Pages: 1-9 DOI: 10.13057/biodiv/d140101

Species diversity of Selaginella in Mount Lawu, Java, Indonesia

AHMAD DWI SETYAWAN1,2,♥, SUTARNO1,3, SUGIYARTO1,3

1Department 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: [email protected]

2Program of Conservation Biology, Department of Biology, Faculty of Mathematics and Natural Sciences, University of Indonesia, Depok 16424, West Java, Indonesia3Program 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 conductedbetween July 2007 and November 2012 on the western and southern slopes of Mount Lawu, Central- and East-Java, Indonesia, withaltitudes 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 foundnine selaginellas species, namely: S. aristata, S. ciliaris, S. involvens, S. opaca, S. ornata, S. plana, S. remotifolia, S. singalanensis andS. zollingeriana.

Key words: species, diversity, taxonomy, Mount Lawu, Java

INTRODUCTION

Mount Lawu, or Gunung Lawu, is a massive compoundstratovolcano, straddling the border between Central Javaand East Java, Indonesia (Lat: 7.625°S, Long: 111.192°E).The north side is deeply eroded and the eastern sidecontains parasitic crater lakes and parasitic cones. MountLawu has long been inactive, but still shows volcanicactivity, where there is a fumarolic area on the south flankat 2,550 m. The only reported activity of Mount Lawu tookplace in 1885, when rumblings and light volcanic ash fallswere reported (GVP 2012). Geologically, the mountain isdivided into two parts, the northern part commonly knownas Mount Lawu (3265 m) is the new Lawu, while thesouthern part known as Jobolarangan Hill (2298 m) is theancient Lawu (Puslitbang Geologi 1992; Pratiwi 2011).Forest fires regularly occur in Mount Lawu. The latestincident was the destruction of 500 hectares of forest at theend 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 approximately20,400 ha (Sriyanto 2003) or 24,188 ha (BLI 2004). Themain area of the forest is managed by Lawu DS ForestManagement Unit (consisting of North Lawu: 5354.7 haand South Lawu: 5719.4 ha), and the rest is managed bySurakarta Forest Management Unit (Kesatuan PengelolaanHutan; KPH). There are two nature conservation areas inthe mountain, namely: Grojogansewu Natural RecreationPark (Taman Wisata Alam; TWA) established by theMinistry of Agriculture decree No. 264/Kpts-Um/10/1968dated October 12, 1968 covering an area of 64.30 ha; and

KGPAA Mangkunagoro I Grand Forest Park (formerlyNgargoyoso Grand Forest Park; Taman Hutan Raya(Tahura) Ngargoyoso) established by the Ministry ofForestry and Plantations decree No. 849/Kpts-II/1999 datedOctober 11, 1999 covering an area of 231.3 ha. At thistime, grand forest park is proposed to be expanded to reachapproximately 1000 ha, covering Karanganyar andWonogiri, Central Java (Slamet, Office of Forestry, CentralJava Province, 2012, pers. com.).

Mount Lawu has an important function for theprotection of natural resources and ecosystems. This area isa buffer zone that limits the distribution of dry-typeecosystems in eastern Java and wet-type ecosystem inwestern Java. Mount Lawu is one of the western distributionborders of Casuarina junghuhniana Miq. (Pinyopusarerkand Boland 1995), and of the eastern distribution borders ofSchima wallichii (DC.) Korth., although this later species isprobably non-native in Mount Lawu (Steenis 1972).Several studies on plant diversity in Mount Lawu havebeen conducted, for example: fungi (Ilyas 2007),cryptogamae (Setyawan and Sugiyarto 2001),spermatophytes (Sutarno et al. 2001), epiphytic plants(Setyawan 2000), epiphytic orchids (Marsusi 2001; Yuliaet al. 2011), epiphytic medicinal plants (Samsali 2008),fruit plants Rubus (Setyawan 1999), medicinal herbPlantago major (Sugiyarto et al. 2006), Vanda tricolororchid (Suparno-Putri 2013), home-garden plants (Harsono2001), plants of Cemorosewu (Khussurur 2006), etc. Thisregion has been proposed as a national park (Setyawan andSutarno 2000; Setyawan 2001; Sriyanto 2003; Setyawan andDirgahayu 2005; WDPA 2010).

BIODIVERSITAS 14 (1): 1-9, April 20132

Selaginella is one of the genera that live in MountLawu. This plant lives in moist environment and requireswater for fertilization. Mountainous region with humidclimate and abundant water sources throughout the year isa hotspot for its diversity. Research on species diversity ofSelaginella in Mount Lawu had never been conductedbefore, but there have been reports of the presence of S.ornata (Setyawan and Sugiyarto 2001) and S. opaca(Setyawan 2009). The observation on the HerbariumBogoriense (BO) collections have found three Selaginellaspecies of Mount Lawu, namely: S. aristata, S. opaca, andS. involvens (ADS 2012, pers. obs.).

A large number of Selaginella species aremorphologically polymorphic and have high morphologicalsimilarity among species; Selaginella is a difficult genus tobe classified (Setyawan et al. 2012). This confusion led toalmost every species having more than one name, even S.ornata and S. involvens, which have high morphologicalvariation, each having more than 25 synonyms (Kesslerand Swale 2008). Nowadays, there are 700-750 recognizedspecies around the world, while more than 200 species arefound in Nusantara (Malay Archipelago), 25 species inJava (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 humidplaces and requires water for fertilization, it becomesinteresting for studying the biodiversity and the climatechange. This study aimed to determine the diversity ofSelaginella 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 ofSelaginella have been conducted in Mount Lawu and theadjacent areas, with altitude between 1100 and 2100 ma.s.l., both in the wet and dry seasons. The research siteswere grouped into three divisions, namely: (i) Protectedforest of Cemorosewu (1600-2100 m a.s.l.), (ii)Grojogansewu Natural Recreation Park (1100-1400 ma.s.l.), and (iii) KGPAA Mangkunagoro I (Ngargoyoso)Grand Forest Park (1100-1500 m a.s.l.). Survey sitesindicating the presence of Selaginella was shown in Table1 and Figure 1.

All three sites are influenced by human activities.Selaginella is generally found in places that are moist andshady, such as roadside cliffs, footpaths and tributriescliffs. Some species can also grow in relatively open sites,such as forest stands of pine (Pinus merkusii), thesettlements and agricultural land. Selaginella rarely growsunder a dense clumps of herbs or shrubs; that place doesnot provide space and light for growth. The southern andwestern slopes of Mount Lawu – where this research wasconducted – has Andisol soil type (Sargiman 1990;Sarifuddin 1998; Jubaedah 2008). This clay soil type hasrelatively higher ability to hold water and nutrients thanpyroclastic sandy soil in the northern and eastern slopes.

All Selaginella species were recorded and collected asherbarium specimen and living collection for theexperimental 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) Species diversity

Protected forest of Cemorosewu and the vicinity (1600-2100 m)Cemorokandang -7.665113° 111.181350° 1807 S. opaca, S. remotifoliaCemorosewu-1 -7.656752° 111.195046° 2070 S. opaca, S. remotifoliaCemorosewu-2 -7.667108° 111.191757° 1876 S. opacaCemorosewu-3 -7.670575° 111.193019° 1633 S. opacaCemorosewu-4 -7.664144° 111.197845° 1915 S. opaca, S. remotifoliaCemorosewu-5 -7.666296° 111.196120° 1865 S. remotifoliaJobolarangan-1 -7.668915° 111.190381° 1754 S. opacaJobolarangan-2 -7.684914° 111.182679° 1884 S. opacaJobolarangan-3 -7.670727° 111.182348° 1753 S. opaca, S. remotifolia

Natural Recreation Park of Grojogansewu and the vicinity (1100-1400 m)Blumbang-1 -7.664726° 111.155295° 1382 S. involvens, S. opaca, S. ornata, S. remotifoliaBlumbang-2 -7.670324° 111.158458° 1464 S. remotifoliaKalisoro -7.663311° 111.152281° 1337 S. remotifoliaTawangmangu-1 -7.661767° 111.143464° 1222 S. zollingerianaTawangmangu-2 -7.660820° 111.136199° 1133 S. zollingerianaTawangmangu-3 -7.660554° 111.139010° 1150 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. remotifoliaNglerak -7.608175° 111.154545° 1556 S. remotifoliaTahura 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. – Selaginella of Mount Lawu, Java 3

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

(768 m a.s.l.). A total of 56 herbarium specimens of ninespecies of Selaginella have been collected from the studysite (Table 1). Each herbarium specimen was unique,distinguished by location and time of collection. Datapassport collected along with the specimens were used asstandard for herbaria specimen. The specimens wereidentified 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); andwere compared with the specimens collection at BO,especially the specimens that had been determined byA.G.H. Alston before; and also by using several newestreferences such as Wong (1982, 2010), Tsai and Shieh(1994), Li and Tan (2005), and Chang et al. (2012). Inaddition to direct observations, we use the literatures toguide the preparation of the description. Meanwhile, theglobal distribution is according to Hassler and Swale(2002).

RESULTS AND DISCUSSION

DescriptionSelaginella 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 brancheson lower part, rooting near base, roll up when dry (S.involvens), branching dichotomously, regularly orirregularly 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 veinsforked), always bearing an inconspicuous ligule on theadaxial side at its base (only prominent in earlydevelopment); vegetative leaves are (tropophyll)monomorphic-spirally arranged at basal main stem anddimorphic-4 lanes arranged on other parts (S. involvens, S.plana), or more often dimorphic and usually arranged intwo median (ventral) and two lateral (dorsal) rows on thebranches (S. ornata, S. singalanensis); median leaves areusually smaller, and in different shape from the lateralleaves; axillary leaves are single borne at the forking ofeach branch, being somewhat different from other leaves.Strobilus (clusters of imbricating sporophylls) are usuallyborne 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 monomorphicor adjacently different, slightly or highly differentiatedfrom vegetative leaves. Sporangia are short-stalked,

C

B

A

KARANGANYAR

WONOGIRI

MAGETAN

NGAWI


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 roundor oval, opening by a transverse slit.

Selaginellaceae Reinch. is a family with only one genusnamely Selaginella P. Beauv., cosmopolitan fern allies,consisting of about 700-750 species; 200s species inNusantara, 25 species in Java, and nine species in MountLawu (Table 2). The results indicated that - at an altitude of1100 to 2100 m - getting to the top, the number of collectedSelaginella species decreased (Table 2). This suggests thatthe distribution of Selaginella is affected by altitude. Atotal of 9 species were found in Grojogansewu (1100-1400m), 6 species in Ngargoyoso (1100-1500 m), and only twospecies in Cemorosewu (1600-2100 m). Altitude of 2100 mseems to be the upper limit of Selaginella distribution;therefore it is very interesting to conduct similar research atan altitude below 1100 m, and to know the distributionshift of Selaginella from the coastal area to the summit ofMount Lawu. Besides, a large number of species found inGrojogansewu are also allegedly associated with the localphysiography. This area has a lot of high cliffs and smallrivers, making it very suitable for the growth ofSelaginella. In Java, the altitude of 1500 m may be theupper 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 isprobably the upper limit for the spread of S. opaca and S.remotifolia.

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

Species

Gro

joga

nsew

u(1

100-

1400

m)

KG

PA

AM

angk

unag

oro

I(N

garg

oyos

o)(1

100-

1500

m)

Cem

oros

ewu

(160

0-21

00 m

)

Tot

al h

erba

ria

spec

imen

t

S. aristata ● ● 4

S. ciliaris ● ● 4

S. involvens ● 4

S. opaca ● ● ● 16

S. ornata ● 3

S. plana ● 3

S. remotifolia ● ● ● 14

S. singalanensis ● ● 4

S. zollingeriana ● ● 4

Total 9 6 2 56

Note: Each herbarium specimen was unique, distinguished bylocation 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 ........................................... 33. Stem fleshy ...................................... S. aristata3. Stem fragile ...................................... S. ornata

2. Stem longer than 30 cm ........................................... 44. Stem hard, caulescent, easily broken ..............

......................................................... S. involvens4. Stem tough ......................................... S. plana

1. Stem creeping, rooting at intervals .............…..…….…… 55. Stem shorter than 15 cm ........................................... 6

6. Leaves ovate to rounded ...................... S. ciliaris6. Leaves lanceolate ....................... S. zollingeriana

5. Stem more than 15 cm ............................................. 77. Stem fleshy .......................................... S. opaca7. Not so ................................................................ 8

9. Leaves loosely arranged ......... S. remotifolia9. Leaves imbricate ............... S. singalanensis

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 decumbentto ascending, dendritic branched, especially at the matureones, ca. 4-20 cm long, 3-6 mm wide (including leaves).Rhizophores are present at basal stem, originated from theventral 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 closelyarranged at the branches, vein single; lateral leaves arelanceolate to oblong-ovate at main stem, lanceolate tofalcate at branches, 1.8-3 mm long, 1-2 mm wide, basesubcordate or rounded, asymmetrical, apex acute or obtuse,margin serrulate to subentire; median leaves are smallerthan the lateral ones, lanceolate to ovate, more or lesssymmetrically, 1.2-2 mm long, 0.5-1 mm wide, baseobtuse, apex caudate to long tail-like, apices are upward orbended back, margin serrulate, single vein reaching theapex; axillary leaves are lanceolate to ovate, 1.5-3 mmlong, 0.5-1.5 mm wide, single vein nearly reaching theapex, 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 cmlong.

Locality: Grojogansewu, NgargoyosoHabitat and ecology: it was found on steep cliffs, at the

edge of the ditch/irigation water, and up to the stream thatflows into Grojogansewu waterfall. It was also found onthe cliff edge of the dirt- and cemented road to the Tahuraoffice shaded by pine and secondary forest, only abundantin 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 arerecumbent, without a significant main stem, 4-5 mm wide(including leaves). Rhizophores are present at intervals but


mostly near the base, originated from the lateral side ofbranching 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 lesssymmetrical, 1.5-2 mm long, 0.6-1 mm wide, base roundedor subcordate, apex acuminate or acute, margin serrulate orciliate, single vein reaching the apex, keeled, pointingoutwards; median leaves are ovate to falcate, asymmetrical,2-2.5 mm long, 0.6-1.5 mm wide, base rounded, apexacute, attenuate or cuspidate, margin serrulate but laciniateat basal part, pointing upwards, minutely toothed, ciliate,midrib prominent, single vein reaching or nearly reachingthe apex; axillary leaves are lanceolate to ovate, equallysided (bisymmetrically), 1.8-2.5 mm long, 1-1.5 mm wide,single vein reaching or nearly reaching the apex, baserounded to subcordate, ciliate, apex acute, margin toothed,laciniate at basal part and serrulate at apical part. Strobilusare solitary or twin, terminal, flattened, complanate, up toca. 1.5-2 cm long;

Locality: Grojogansewu, NgargoyosoHabitat and ecology: It was found on the steep cliff, at

the edge of the irigation water, and up to the stream thatflows into Grojogansewu waterfall. It was also found onthe cliff edge of the cemented road to the Tahura office

shaded by pine and secondary forest, not recorded in thedry 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, NorthernAustralia, 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 stoloniferousrhizome, without branches on the lower half, from a verywidely 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.

D E F

H

C

G

BA

I


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 whenerect; creeping stems when subterranean. Leaves aremonomorphic, colorless, scales ovate ciliate, sessile, apexacute, apprised or recurved; erect branches dendritic, fan-shaped, up to more than 40-50 cm long, 1-1.5 mm in diam.,with several dormant buds or leaves on lower part of mainstem, monomorphic but dimorphic on much branchingparts. Rhizophores are absent. Leaves of the basal mainstem are monomorphic, ovate, clasping, nearlyasymmetrical, 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 theauricule, arose and long ciliate towards apex. Leaves on thebranches are dimorphic, arranged in 4 lanes (2 lateral, 2median), vein single, reaching the apex; lateral leaves arelanceolate to ovate, asymmetrical, 0.8-2.5 mm long, 0.3-1.5mm wide, ciliate near base, base oblique with auriculate,apex attenuate or acuminate, vein single always curved andpointing to abaxial side, having 2 significant groovesbeside the vein, adaxial blade raised and forming two-main-vein, margin laciniate but spinose at the auricule;median leaves are ovate on the main stem but elliptical orlaceolate to ovate on the top branch, asymmetrical, 1.5-3mm 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 theadaxial surface beside the vein of median leaves on the topbranch, having 2-3 grooves at the abaxial surface on the topbranch, 2 beside the vein and 1, less significant or absent,inside the midrib, margin entire to serrate, laciniate at mostbasal part of margin, concentrated spinose at the miniature-auricle base, minutely ciliate, pointing upwards; axillaryleaves are ovate to cordate on first forked site butlanceolate to ovate at following forked site, asymmetrical,1-2.5 mm long, 0.5-2.5 mm wide, base subcordate orcordate, apex acute or attenuate, margin serrate butlaciniate at basal part, minutely ciliate. Strobilus aresolitary, terminal, tetragonal, up to more than 2 cm long.

Locality: GrojogansewuHabitat and ecology: It was found on the steep cliff, at

the edge of the irigation water and small stream, at altitudeof 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 toascending, usually fertile branches alternate on long fleshymain stem, up to 80 cm long, 3-8 cm wide (includingleaves). Rhizophores are at the branching stem, mostly nearthe base, originated from the dorsal side of stem at thebranch site, ca. 1-1.5 mm in diam. Leaves on the main stemare monomorphic, oblong, asymmetrical, spaced fartherapart than their width, midrib present. Leaves on thebranches are dimorphic, arranged in 4 lanes (2 dorsal, 2

ventral), loosely arranged at long creeping stem but closelyarranged 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 mmlong, 1-2 mm wide, base obliquely cordate or cordate, apexcaudate, pointing upwards, imbricating at the ends ofbranches, vein single not reaching the apex, marginserrulate or serrate, but entire at basal part; axillary leavesare ovate, entire, rounded or obtuse, symmetrical, 2.5-3.5mm long, 1.5-2.5 mm wide, apex acute, margin entire orserrulate at apical part. Strobilus are solitary, terminal orlateral, tetragonal, up to more than 3.5 cm long.

Locality: Grojogansewu, Ngargoyoso, CemorosewuHabitat and ecology: It was found on the steep cliffs

and river bank above the channel irrigation and small riverto Grojogansewu waterfall, on the cliff at the edge of thedirt-road and cemented road to the Tahura office shaded bypine and secondary forest, on the cliffs on the river banksnear the bridge and new highway, along the footpath andthe cliffs from Cemorosewu to Grojogan kembar waterfall,on the edge of several small springs near the campingground, on the small tributaries in Jobolarangan Hills, onthe cliff above the old road of Cemorokandang toSarangan, on the trekking lane above Cemorosewu, nearthe field that made after forest fire. It could be foundthroughout the year; at altitude of 1150-2070 m a.s.l. Thisspecies is mostly found near S. remotifolia

Distribution: Sumatra, Java, Lombok, Ceram, NewGuinea, Philippines

Selaginella ornata (Hook & Grev.) Spring; Bull. Acad.Brux. 10: 232 (1843) (Figure 2E)

It is a fragile perennial herb, greenish or brownish ingeneral appearance. Stems are suberect fragile, very easilybroken, 20-30 cm long, 1-3 cm wide (including leaves).Rhizophores are at the lower part and sometimes atbranching stem, originated from the dorsal side of stem atthe branch site, ca. 0.5-1 mm in diam. Leaves aredimorphic, arranged in 4 lanes (2 dorsal, 2 ventral), denselyarranged throughout the stem and imbricating at top ofbranches; lateral leaves are oblong to falcate, denticulate todentate, exauriculate, asymmetrical, 1.5-3 mm long, 1-1.5mm wide, apex acuminate to acute, and prickly tip, veinsingle 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, 0.5-1 mm wide, apex acute, base rounded, margin entire.Strobilus are solitary, terminal, bisymmetrical, upper-plane,up to more than 1 cm long.

Locality: GrojogansewuHabitat and ecology: It was found the steep cliffs above

a small irigation channel and tributary of Grojogansewuwaterfall, on the cliffs on the small river banks near the


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 withstoloniferous rhizome, without branches on the lower part,ascending from a subterranean trailing base, up to 80-100cm long, 3-10 cm wide (including leaves); subterraneanstems (rhizome) shallowly radiating. Rhizophores aresometimes at the branching stem, originated from thedorsal 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 oracute, but rounded tip, asymmetrical, margin translucent,entire. Leaves on the branches are dimorphic, arranged in 4lanes (2 dorsal, 2 ventral), loosely arranged at lower stembut closely arranged at branches; lateral leaves are oblongto ovate, asymmetrical, 2-4.5 mm long, 2-3 mm wide, apexacuminate 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 tooblong, asymmetrical, 1.5-3 mm long, 1-2 mm wide, apexacuminate 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, apexacute, minutely ciliate, base rounded, margin entire.Strobilus are solitary, terminal, tetragonal, up to more than3 cm long.

Locality: GrojogansewuHabitat and ecology: It was found on the steep cliffs

above a small irrigation channel and tributary ofGrojogansewu, remaining abundant in the dry season,altitude 1150 m a.s.l.

Notes: It is originally low-lying vegetation, and 1200 maltitude in Turgo (Mt. Merapi) is probably the highest pointthat 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, CostaRica, 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, usuallyseveral fertile branches alternate on long main stem, up to100 cm long, 0.5-1 cm wide (including leaves).Rhizophores are at the branching stem, originated from thedorsal 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 theirwidth, midrib present. Leaves on the branches aredimorphic, arranged in 4 lanes (2 dorsal, 2 ventral), loosely

arranged at the long creeping main stem but closelyarranged at branches; lateral leaves are contiguous,lanceolate to ovate, asymmetrical, 1.5-3 mm long, 1-2 mmwide, apex acute to acuminate, vein single, obscure notreaching the apex, base rounded, margin serrulate butusually entire or minutely ciliate, pointing outwards; .median leaves are lanceolate to ovate, asymmetrical, 1.5-2.5 mm long, 0.5-1 mm wide, base obliquely cordate orcordate or cuneate, apex attenuate or caudate, leaves atends of branches imbricating, vein single not reaching theapex, margin serrulate or serrate, but entire at abaxialmedium and basal part; axillary leaves are ovate, entire,rounded or obtuse, symmetrical, 2-2.5 mm long, 1-1.5 mmwide, apex acute, margin entire or loosely serrulate atapical part. Strobilus are solitary, terminal or lateral,tetragonal, up to more than 2 cm long.

Locality: Grojogansewu, Ngargoyoso, CemorosewuHabitat and ecology: It was found on the steep cliffs and

river bank above the channel irrigation and small rivertowards Grojogansewu waterfall, on the cliff at the edge ofthe dirt-road and cemented road to the Tahura officeshaded by pine and secondary forest, among pine stand ofTahura forest, on the cliffs on the river banks near thebridge and new highway, and around the vegetable fields,along the footpath and cliffs from Cemorosewu toGrojogan Kembar waterfall, on the edge of several smallsprings near the camping ground, cliff above the old roadof Cemorokandang to Sarangan, on the trekking lane aboveCemorosewu, near the field made after forest fire. It grewthroughout the year but decreased at dry season; at altitudeof 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 andvery thin, 20-25 cm long, 1-3 cm wide (including leaves).Rhizophores are at branching stem, originated from thedorsal side of stem at the branch site, ca. 0.5 mm in diam.Leaves are dimorphic, very soft, arranged in 4 lanes (2dorsal, 2 ventral), densely arranged at thorough stem andimbricating at top of branches; lateral leaves are oblong,imbricating, asymmetrical, 1.5-2.5 mm long, 0.5-1.5 mmwide, apex acute, vein single not reaching the apex, baserounded, 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, baserounded, 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 aresolitary, terminal, loosely, bisymmetrical, upper-plane, upto 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 rivertowards Grojogansewu waterfall, on the cliff at the edge of


the cemented road to the Tahura office shaded by pine andsecondary forest. It generally died in the dry season, but ina moist area it could grow throughout the year; at altitudeof 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, fan-shaped; multiple branched at main stem, every branchforming dendritic stem. Stems are ascending, dendriticbranched, especially at the mature ones, ca. 5-15 cm long,3-5 mm wide (including leaves). Rhizophores are onlypresent at lower part, ca. 0.5 mm in diam. Leaves on themain stem are monomorphic, lanceolate, acuminate,asymmetrical, spaced farther apart than their width. Leaveson the branches are dimorphic, arranged in 4 (2 lateral, 2median), loosely arranged at the main stem but closelyarranged at the top branches, vein single; lateral leaves arelanceolate, asymmetrical, 1.5-2 mm long, 0.5-1.5 mm wide,apex acute, base rounded, margin entire; median leaves aresmaller than lateral ones, lanceolate, 1-1.5 mm long, 0.5mm wide, apex caudate to long tail-like, margin entire,single vein; axillary leaves are lanceolate to subcordate, ca1-1.5 mm long, 0.5-1 mm wide, single vein nearly reachingthe apex, apex acute, base rounded, margin entire. Strobilusare 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 thecemented road to Tahura office shaded by pine andsecondary forest, on the roadside on the plastered and dirtdrainage ditch; not recorded in the dry season, at altitude of1150-1222 m a.s.l.

Distribution: Bali, Java

CONCLUSION

Nine species of selaginellas have been found in MountLawu and the adjacent areas, namely: S. aristata, S.ciliaris, S. involvens, S. opaca, S. ornata, S. plana, S.remotifolia, S. singalanensis and S. zollingeriana. Allspecies could be identified based on its vegetative-morphological characteristics.

ACKNOWLEDGEMENTS

We thank the head and staff of Herbarium Bogoriense(BO), RCB-IIS, Cibinong-Bogor, Indonesia for facilitatedthe herbarium materials, the same to the management ofTahura KGPAA Mangkunagoro I Ngargoyoso, TWAGrojogansewu and Perhutani (BKPH Lawu Utara). Parts ofthis work were supported by Featured Research HigherEducation (Decentralization Research Grant) fromDirectorate General of Higher Education, Ministry ofEducation and Culture, RI for fiscal year 2013.

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Endophytic fungi associated with Ziziphus species and new records frommountainous area of Oman

SAIFELDIN A.F. EL-NAGERABI1, ♥, ABDULQADIR E. ELSHAFIE2, SULEIMAN S. ALKHANJARI1

1Department 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: [email protected]

2Department 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 ofOman and new records. Biodiversitas 14: 10-16. Ziziphus species of the family Rhamnaceae grow extensively in arid and semi-aridregions. It is possible that the endophytic fungi associated with this plant might enhance the host resistance to the environmentalimpacts. The endophytic fungal population inhabiting the healthy leaves of Z. spina-christi and Z. hajanensis plants were determinedfrom April 2008 to October 2011. The endophytic fungal communities varied between the two species, and 45 fungal species, 18 sterilemycelia 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 arenew to Ziziphus plants and 45 species are new to the mycoflora of Oman, whereas 27 species are new to Arabian Peninsula. The genusAlternaria 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 Phomasorghina (3%). The recovery of many fungal isolates, morphologically various sterile mycelia and yeasts suggests the high biodiversityof the endophytes invading these plants with strong evidence for future isolation of numerous fungal species through adopting moreadvanced 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 attractingdifferent interests of the world. They cover 24% of theearth surface and support 12% of the world population asan excellent source for water. They are inhabited by diverseflora and fauna (Anon 2008). In Oman, Al-Jabal Al-Akhdarin the Western Hajer mountains (1500 m) is a globallydistinguished ecosystem having various climatic conditionsand diverse vegetation. It has experienced rapiddevelopment which is associated with noticeable climaticchanges and vegetation deterioration. The problem is notlimited to conspicuous flora and fauna, but extends to fungiand bacteria which depend on higher plants for theirsurvival (Carlile et al. 2001).

Ziziphus also known as “Sedra” is an important genusof the family Rhamnaceae found growing extensively inarid and semi-arid regions and represented by 135-170species (Bhansali 1975; Mathur and Vyas 1995; Maraghniet al. 2010). Of these, only Z. spina-christi (L.) Wild and Z.hajanensis are common species inhabiting Al-Jabal Al-Akhdar and are indigenous to Oman with a wide ecologicaland geographical distribution growing under variety ofenvironmental 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). Recentlythe anti-inflammatory analgesic and antispasmodicactivities were reported in rodents (Borgi et al. 2008; Borgiand Chouchane 2009).

Numerous and diverse fungi were isolated from thetissues of most parts of terrestrial and aquatic plantsspecially the leaves as endophytes (Huang et al. 2008).Endophytes are fungi or other microorganisms which spendat least part of their life cycle inside leaf tissues withoutcausing 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 andimprove the ecological adaptability of the host byenhancing plant tolerance to environmental stress andresistance to phytopathogens and/or herbivores (Clay andSchardl 2002; Waller et al. 2005; Barrow et al. 2007; Liu etal. 2010; Sun et al. 2011). Therefore, the alteration ofbeneficial endophytes could lead to the development ofnew and devastating disease to the host plant (Mmbaga andSauve 2009). These endophytes produce innumerable andvaluable novel secondary metabolites (Strobe 2002). Theyare an excellent source of a therapeutically important classof metabolites (Pietra 1997).

EL-NAGERABI et al. – Endophytic fungi associated with Ziziphus 11

Worldwide, many researchers are collecting andisolating fungi from unexplored sites, habitats andsubstrates, particularly in extreme environmentalconditions (Ilyas et al. 2009). However, of all world plants,it seems that only a few species have had their completecomplement of endophytes studies (Strobel 2002; Huang etal. 2008). The variations of endophytes are due in part togeneric differences among plants and the variations inenvironmental conditions (Elamo et al. 1999). In Oman, theresearch carried out until now focused on coprophilousfungi (Gene et al. 1993; Elshafie 2005), mycotoxins andmycotoxigenic moulds (Elshafie and Al-Shally 1998;Elshafie et al. 1999, 2002), nematophagous fungi (Elshafieet al. 2003, 2005), and some plant diseases (Elshafie andBaomer 2001; Al-Bahry et al. 2005). There are few studieson some plant diseases of cultivated crops in different areasof Oman, nonetheless, there is no single study on thebiodiversity of the fungal flora of the wild and cultivatedplants of Al-Jabal Al-Akhdar . It is evident that endophytesare among a poorly understood group of fungi (Gazis andChaverri 2010). It is quite promising to explore interestingendophytic fungal species among the myriad plantsincluding the main two species of the genus Ziziphusnamely Z. spina-christi, and Z. hajanensis which havenever 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 duringthe growing seasons, between April 2008 and October2011, in the mountain of Al-Jabal Al-Akhdar, and the

seasonal variation, biological diversity, and species-specificity of these endophytes in the leaves of the twoselected plant species were evaluated.


Sampling siteThis study was carried out in Al-Jabal Al-Akhdar

mountain, Oman (Figure 1), which is located at the Southof the Arabian Gulf. It is bordered by Yemen on the South,the Arabian Sea on the Southeast, Iran on the Northeast, theUnited Arab Emirates on the Northwest, and Saudi Arabiaon the West. It lays between latitude of 21°00,N - 29°00,Nand longitude of 51°00,E - 59°40,E. The climate variesaccording to variation in geographical regions which is hot-dry in the interior, hot-humid in the coastal area and humidin the South with summer monsoon rain. The averagetemperature is about 26°C with annual precipitation of lessthan 100 mm (AlKhanjari 2005). Al-Jabal Al-Akhdar in theWestern Hajer mountain range above 1500 m with averagetemperature on the plateau of 18.5°C which is much lowerthan that in the surrounding region (29°C) and relativehumidity of 46%.

Plant materialsEighteen samples of healthy green leaves from two

different stands of Ziziphus spina-christi and Z. hajanensis

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


were collected at the same elevation of Al-Jabal Al-Akhdarmountain, Oman. The selected plants were identified at theDepartment of Biological Sciences and Chemistry, Collegeof Arts and Sciences, University of Nizwa, and Departmentof Biology, College of Science, Sultan Qaboos University.Samples from 10 different plants were collected at differenttimes and seasons between April 2008 to October 20011(Table 1). The samples were kept in sterile polyethylenebags and stored in refrigerators at 5°C to be used for theisolation of the endophytic fungi.

Table 1. The collection date and plant material samples used forisolation of endophytic fungi from Ziziphus spina-christi and Z.hajanensis

Sample Nos. Tissues used for isolation Sample date

SM1 Green leaf 4-2008SM2 Green leaf 6-2008SM3 Green leaf 9-2008SM4 Green leaf 12-2008SM5 Green leaf 3-2009SM6 Green leaf 5-2009SM7 Green leaf 9-2009SM8 Green leaf 11-2009SM9 Green leaf 1-2010SM10 Green leaf 3-2010SM11 Green leaf 5-2010SM12 Green leaf 7-2010SM13 Green leaf 9-2010SM14 Green leaf 12-2010SM15 Green leaf 3-2011SM16 Green leaf 5-2010SM17 Green leaf 7-2010SM18 Green leaf 10-2011

Isolation of endophytic fungiThe green leaves of the selected plant were cut into

small pieces of 10 mm in length and washed with severalchanges of sterile distilled water. The pieces were surfacedisinfected 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 asepticallyinoculated on Potato Dextrose Agar (PDA, Potato, 200g;dextrose, 20g; agar 15g; distilled water, 1L) supplementedwith chloramphenicol (0.05 mg/ml) to inhibit the bacterialgrowth, until the mycelia appeared surrounding the planttissues. The inoculated plates were incubated at theambient temperature (27-29°C) for 7-10 days until themycelial growth was apparent on the media. The fungalcolonies which developed on the tissues were theninoculated on Malt Extract Agar (MEA) for preparation ofpure colonies and further identification and preservation asdry herbarium materials at the herbaria of Department ofBiological Sciences and Chemistry, College of Arts andSciences, University of Nizwa, and Department of Biology,College of Science, Sultan Qaboos University.

Identification of endophytic fungiThe isolated endophytic fungi were identified using

macroscopic features based upon colony morphology on

the growth media and microscopic observations of myceliaand asexual/sexual spores according to the methoddescribed in literature, and consulting many taxonomicbooks and numerous monographs (Barnett 1955; Raper andFennell 1965; Kobayashi 1970; Pitt 1979; Ellis 1971, 1976;Sutton 1980; Webster 1980; Nelson et al. 1983; Samson etal. 1995; Barnett and Hunter 1998, 2003; Barac et al. 2004).

Data analysisThe number of cases of isolation (NCI) of each fungal

species was calculated according to modified formula ofGazis and Charerril (2010) as the number of the samplesfrom which the fungus was isolated, whereas theoccurrence remarks (OR) as a total number of the samplesfrom which a given species was isolated compared to thetotal number used for the isolation of the fungi. Thenumber of the samples from which a given species wasisolated divided by the total number of the samples wasused to calculate the percentage incidence of fungal speciesin each genus.


Biodiversity of endophytic fungiFifty two species belonging to 21 genera of fungi in

addition to unidentified 29 sterile mycelia and 17 yeastswere isolated from the green leaves of two Ziziphus speciesplants (Z. spina-christi, Z. hajanensis) (Table 2). Of theseisolates, 45 species, 18 sterile mycelia and 12 yeasts wereisolated form Z. spina-christi, whereas 35 species, 11sterile mycelia and 5 yeasts were recovered from Z.hajanensis. The highest number of species were recoveredfrom the genus Alternaria (9 species), followed byDrechslera (7 species), Aspergillus and Fusarium (6species), 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 unidentifiedisolates from the genera of Aspergillus, Dissophora,Fusarium, and Penicillium. The species of the genusAlternaria was the most predominant genus on the leaftissues and were isolated from 19-81% of the samplescollected at different time of the year. This genus isfollowed 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 (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%).Since there is no previous study on the endophytic fungi ofZiziphus plants, the whole fungi isolated in the presentinvestigation are new records to these plants, whereas 45species were reported for the first time in the mycoflora ofOman and 27 species are new to the mycoflora of ArabianPeninsula (Table 2).


Table 2. Number of cases of isolation (NCI, out of 18 samples),occurrence remarks (OR) and incidence percentage (I%) ofendophytic fungi of Ziziphus spina-christi and Z. hajanensis

Z. spina-christi

Z.hajanensisIsolates Record

type NCI OR NCI OR

I%

Alternaria alternata ®* 18 H 7 M 69Alternaria chlamydospora ® 13 H 6 M 53Alternaria cheiranthi ® Ψ 7 M - - 19Alternaria cineraniae ® Ψ 5 L - - 14Alternaria citri ® Ψ 16 H 4 L 56Alternaria pluriseptata ® Ψ 18 H 11 H 81Alternaria radicina ® Ψ 14 H 9 M 64Alternaria tenuissima ® 16 H 12 H 78Alternaria triticina ® Ψ 11 H - - 31Alysidium resinae ® Ψ 4 L - - 11Anguillospora longissima ® Ψ 3 L - - 8Arthrinium sp. ® 1 R - - 3Aspergillus spp. ® 7 M 5 L 33Aspergillus caespitosus ® Ψ 5 L 2 R 19Aspergillus flavus ®* 14 H 8 M 61Aspergillus fumigatus ®* 16 H 4 L 56Aspergillus niger ®* 18 H 10 H 78Aspergillus unguis ® Ψ 8 M 2 R 22Aspergillus wentii ® 6 L 2 R 19Bactrodesmium rahmii ® - - 3 L 8Catenularia state ofChaetosphaeria innumera

® Ψ 2 R 1 R 8

Cladosporium spp. ® 8 M 3 L 31Cladosporium chlorocephalum ® Ψ - - 5 L 14Cladosporium cucumerinum ® 6 M - - 19Cladosporium sphaerospermum ® 3 L - - 11Cladosporium tenuissimum ® 12 H 8 M 56Curvularia harveyi ® Ψ 3 L - - 8Curvularia intermedia ® Ψ 5 L 2 R 19Curvularia lunata ®* 10 H 8 M 50Dendryphiella infuscans ® Ψ 2 R - - 6Dissophora sp. ® Ψ 1 R - - 3Drechslera australiensis ® 10 H 6 M 44Drechslera biseptata ® Ψ 5 L 3 L 22Drechslera hawaiiensis ® 9 M 7 M 44Drechslera indica ® Ψ 6 M 4 L 28Drechslera ravenelii ® Ψ 4 L - - 11Drechslera spicifera ®* 11 H 8 M 53Drechslera cactivora ® Ψ - - 5 L 14Fusarium spp. ® 5 L 3 L 22Fusarium chlamydosporum ® 7 M 5 L 33Fusarium lateritium ® 3 L - - 8Fusarium merismoides ® Ψ 2 R - - 66Fusarium nivale ® 6 M - - 17Fusarium reticulatum ® 3 L - - 8Fusarium sambucinum ® 4 L 1 R 14Hansfordia biophila ® Ψ - - 2 R 6Hansfordia pulvinata ® Ψ - - 1 R 3Helminthosporium sorghi ® Ψ 2 R - - 7Penicillium spp. ® 6 M 2 R 22Penicillium chrysogenum ® 2 R - - 6Penicillium purpurogenum ® 3 L 1 R 11Penicillium citrinum. ® 5 L 3 L 22Phoma sorghina ® 1 R - - 3Rhizopus stolonifer ®* 15 H 13 H 78Trichocladium canadense ® Ψ - - 4 L 11Trichodochium disseminatum ® Ψ - - 2 R 6Ulocladium alternariae ® Ψ 7 M 4 L 31Ulocladium consortiale ® 4 L 1 R 14Yeasts * 12 H 5 L 47Sterile mycelia ® 18 H 11 H 69Note: *: Known to mycoflora of Oman; Ψ: New record to ArabianPeninsula; ® New record to the Ziziphus spp.; OR: Occurrenceremarks, 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, areexcellent reservoirs of several types of microorganismsincluding numerous endophytic fungi (Petrini 1991;Bokhary et al. 2000). Therefore, many fungal species werecontinuously isolated from the tissues of the most parts ofterrestrial and aquatic plants (Devarajan et al. 2002; Huanget al. 2008). These fungi represent an important andquantifiable component of fungal biodiversity and areknown to affect the biodiversity and structures of plantcommunities (Krings et al. 2007; Huang et al. 2008).Several studies of endophytic fungi from tropical andtemperate forests support the high estimate of speciesdiversity (Kumar and Hyde 2004; Santamaria and Bayman2005; Santamaria and Diez 2005; Sänchez Märquez et al.2007). Almost all the terrestrial plants studied havemitosporic, ascomycetes fungi and sterile forms asendophytes (Bill 1996; Devarajan et al. 2002). The presentstudy showed that pigmented dematiaceous hyphomycetes(mitosporic fungi) and ascomycetes colonized the tissues ofthese plant species (Table 2). Some of these fungi such asthe species of Alternaria alternata, A. angustiovoide, A.brassicicola, Cladosporium, Helminthosporium, Chaeto-mium, Drechslera, Aspergillus, Fusarium, Penicillium,Phoma, Ulocladium, and Camarosporium were isolated insimilar study of halophytic Suaeda spp. and medicinalplants from China (Huang et al. 2008; Sun et al. 2011). Thedark mycelia of these fungi benefit their host throughabsorption of more UV radiation compared to whitemycelia (Sun et al. 2011). Therefore, these fungi mightenhance the growth and improve ecological adaptation ofthe host plants by enhancing plant tolerance toenvironmental stresses and resistance to phytopathogensand/or herbivores as suggested by many authors (Clay andSchardl 2002; Waller et al. 2005; Barrow et al. 2007; Liu etal. 2010; Sun et al. 2011). Thus, it was suggested that thedark pigmented mycelia increase the host resistance tomicrobes and hydrolytic enzymes (Carlos et al. 2008; Sunet al. 2011).

Normally various fungal taxa were isolated asendophytes from the leaf tissues of single plant species oftropical plants (Petrini 1991). Some of these fungi arepathogenic or saprophytic which under favorableconditions may become pathogenic; while there are otherswhich live on the leaves only as saprophytes and get theirnutrition from exudates of the leaves’ tissues, insectexcretion or from air-borne organic matters deposited onthe surface of the leaves (Last and Deighton 1965; Bokharyet al. 2000). The variations of foliar endophytes are due inpart to genetic differences among trees and the variations inthe environmental conditions (Elamo et al. 1999). In theinvestigation of species composition in woody plants,although large number of endophytes was obtained, fewspecies dominated the community (Petrini et al. 1992).Some species of Alternaria, Colletotrichum and Fusariumhave been reported as endophytes for many plants (liu et al.2010). Phoma, Cladosporium, and Fusarium are frequentlyreported to occur as endophytes in terrestrial plants of thetropics (Brown et al. 1998). Alternaria spp., Cladosporiumspp., Stemphylium spp., and Pleospora sp. were dominantendophytes of Salicornia europaea in Japan (Sun et al.


2011). Alternaria alternata, Cladosporium cladosporioidesand Penicillium chrysogenum are the most commonendophytes isolated from halophytes of the Red Sea Coastof Egypt (El-Morsy 2000). Aspergillus niger was thedominant endophytic fungus in mangrove and legumes(Dorothy and Kandikere 2009). It is evident thatdematiaceous fungi universally inhabit plants in differentecological zones and play important ecological roles for thesurvival of the plants. Generally many species of the genusAspergillus such as A. fumigatus, and A. niger in additionto species of Penicillium and Fusarium are adapted todifferent plant tissues (Ilyas et al. 2009). In the presentstudy, some of endophytic fungi isolated in similar studies(Petrini et al. 1992; Dorothy and Kandikere 2009; Ilyas etal. 2009; Sun et al. 2011) were recovered from the greenleaves of the two species of Ziziphus plants whereas theremaining species were reported for the first time asendophytic fungi on these plant species (Table 2). Theseindicate the endophytic nature of fungi frequently isolatedfrom the green leaves of these two Ziziphus species.

Biodiversity of sterile myceliaSterile mycelia consist of various morphological fungal

types without any true spores. These fungi are considerablyprevalent in endophytic investigations (Lacap et al. 2003;Huang et al. 2008). Of the frequently encounteredendophytic fungal groups, sterile mycelia had the highestrelative frequency (27.2%) (Huang et al. 2008). In thepresent study, 29 sterile mycelia were isolated from thetested samples with the highest occurrence remark andlevel of incidence (69%) (Table 2). These mycelia revealeddifferent macroscopic and microscopic features and do notform reproductive structures when incubated for longperiod of time in order to enhance fungal sporulation. Thissuggests the high possibility of isolating more fungalspecies using advanced identification methods.

Endophytic fungal community among different plantspecies

Many plants are colonized by a characteristic populationof microorganisms (Bowerman and Goos 1991). Endophyticfungi frequently demonstrate single host specificity at theplant species level, but this specificity could be influencedby seasonal changes of the climatic factors (Cohen 2004;Hung et al. 2008; Sun et al. 2011). Partial heterogeneity orgeographic separations were used to indicate theendophytic fungal segregation impacted by environmentaldifferences (Yahr et al. 2006). A recent study showed thatendophytes are not host specific (Jalgaonwala et al. 2011).They colonize multiple host species of the same plantfamily within the same habitat, and their distribution can besimilar in closely related plant species (Huang et al. 2008).A single endophyte or different strains of the same funguscan be isolated from different parts or tissues of the samehost, which indicate their ability to utilize differentsubstrates (Jalgaonwala et al. 2011). These variations inendophyte colonization could be caused by the differencein substrates and nutrients of the host tissues (Rodrigues1994; Rodriguez et al. 2009). The most frequent endophyticfungal 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 differencesin the structural and nutritional composition of the planttissues (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 by31 species of endophytic fungi of variable levels ofoccurrence, whereas 19 species were specific to Z. spina-christi and 7 species were isolated from Z. hajanensis. Theincidence levels of these fungi are evidently higher in thegreen leaves of Z. spina-christi comparable to Z.hajanensis. These indicate the possibility of some degree ofspecies-specificity to these fungi as suggested by manyauthors (Cohen 2004; Hung et al. 2008; Sun et al. 2011)and with similar recovery at different incidence levels ofendophytic fungi in these closely related Ziziphus species(Huang et al. 2008; Jalgaonwala et al. 2011).

Seasonal biodiversity of endophytic fungiLittle is known about the temporal changes in the

endophytic fungal community. The diversity of endophyticfungi recovered from the selected plant is similar duringsummer (March-July) and winter (September-January).Almost the same species of fungi were isolated from thetissues of the plant, and there are no evident variations offungal flora with the seasons. These results showed thatfungal species colonizing the tissues of the plant wereconsistent during the growing seasons. This is may be dueto the continuous growth of the mycelia within the tissuesand production of new spores to invade new tissues (Sun etal. 2011). However, the abundance of endophytes variedamong sampling times and did not increase over time. Onthe other hand, precipitation may influence the incidence ofendophytes (Sahashi et al. 2000; Göre and Bucak 2007).More fungal endophytes developed in plant tissues inspring than in autumn and the higher rainfall in spring mayenhance evidence dispersal of the fungal spores (Göre andBucak 2007). It has been suggested that the smaller and themore scattered the plant fragments sampled, the higher theprobability of approaching real diversity values ofendophytic fungal communities (Gamboa and Bayman2006). Fungal endophytes that colonize healthy planttissues either remain dormant or produce more extensivebut symptomless infections (Devarajan et al. 2002). In thepresent study, there are no apparent seasonal variationsamong of endophytic fungi associated with the two selectedspecies of the genus Ziziphus as concluded in similarstudies (Sun et al. 2011).

CONCLUSION

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


isolation frequencies and occurrence remarks. This studywas conducted using classical taxonomic methods andidentification techniques which do not facilitate theisolation of many fungi and identification of numerousyeasts and sterile mycelia. Therefore, our future studiesshould focus and utilize many molecular techniques whichimprove our research and knowledge of the biodiversity ofthe endophytic fungi.

ACKNOWLEDGEMENTS

We thank the Department of Biological Sciences andChemistry, College of Arts and Sciences, University ofNizwa, and Department of Biology, College of Science,Sultan Qaboos University for providing space and facilitiesto carry this research. We thank the University of NizwaWriting Center for proof reading the English of thismanuscript.

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Dynamics of fish diversity across an environmental gradient in theSeribu 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

1Laboratory of Marine Biodiversity and Biosystematics, Department of Marine Science and Technology Faculty of Fisheries and Marine ScienceBogor Agricultural University. Jl. Agatis No. 1, Bogor 16680, West Java, Indonesia. Tel./Fax. +62 251 8623644, e-mail: [email protected].

2Office 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 ofSeribu Islands have been affected by multitude of anthropogenic pressures. However, the biodiversity of reef fishes across thearchipelago linked to environmental condition is poorly known. This study aimed to investigate the biodiversity and the trophic level offish communities across the archipelago. The study on reef fish communities was conducted on 33 reef sites associated with islands orshoal randomly chosen from each zone along environmental gradients from the inshore water nearest of Jakarta Bay to the offshorewater 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 offish abundance using the Bray Curtis similarity index and non-metric multidimensional scaling (MDS) clearly showed the clustering ofsub-districts, near and far from Jakarta Bay. The results showed that the sub-districts can be clustered into three groups. Group oneconsists 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, Kelapa) located in mid of the archipelago. The third group consists of one sub-district (Harapan) located inthe northern part of the Seribu Islands. Based on species richness and fish diversity indices, the sub-districts can be clustered into twogroups (1 = Pari and Tidung, 2 = Panggang Kelapa, Harapan). However, levels of similarities among sub-districts varied. The fishcommunity in sub-district of Pari was dominated by carnivorous, omnivorous and herbivorous fishes, while those in the rest of sub-districts were dominated by omnivorous and carnivorous fishes. The present study results showed that the biodiversity of reef fishesacross 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 humanactivities through pollution and habitat loss throughout theworld (Burke et al. 2011), and sea level rise or the increaseof ocean temperature due to the global change (Hughes etal. 2003). In Indonesia, marine communities have beenimpacted by an increase in eutrophication andsedimentation levels as shown in the waters of Jakarta Bay(Verstappen 1988; Marques et al. 1997; Renema 2008). Asa result of increased sedimentation, nutrient loading, andchemical contamination, coral reefs became degraded(Rees et al. 1999; Williams et al. 2000). Furthermore, reefdegradation could affect the coral reef fish communitiesdue to their strong relationship.

The Seribu Islands (or Thousand Islands, KepulauanSeribu), which consists of 110 islands spread from theJakarta Bay to as far as 80 km to the north of the Java Sea,have been threatened by different kinds of anthropogenicpressures including coral mining, fishing, anchor damage,oil spills, resort construction and the discharge of industrial

and domestic effluents (Rees et al. 1999; Rachello-Dolmenand Cleary 2007; Willoughby 1986; Uneputty and Evans1997). In the 1980s, the archipelago reefs also experiencedbleaching phenomenon due to ENSO (El Niño SouthernOscillation) resulting in the death of mainly branchingspecies of the genera of Acropora and Pocillopora (Brownand Suharsono 1990).

Regions of the Seribu Islands are divided into threezones according to environmental gradient from the inshorewater of Jakarta Bay to the offshore water of the outerislands (Hutomo and Adrim 1985). Since reef studies in1920s, the reefs surrounding Onrust Island, located inJakarta Bay, have been excluded from reef studies due tomeasurable anthropogenic influences (Zaneveld andVerstappen 1952). The environmental pressures on JakartaBay have increased until today and have been noted inseveral studies (e.g. Tomascik et al. 1997). A number ofstudies also show that reef coverage in Jakarta Bay is verylow and shifts toward the Seribu Islands, as a result ofdiminishing human activities and pollution (Verstappen1988; Cleary et al. 2006).


The gradient of environmental quality has changed themarine 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 coralreefs and spatial variability affect the trophic structure ofthe fish community. For instance, the decrease of livecorals has increased the coverage of algae which in turngives benefit to herbivorous fishes (Madduppa et al. 2012).Therefore, the current study aimed to investigate thebiodiversity dynamics and the trophic levels of fishcommunities across the archipelago.


Study sitesThe Seribu Islands Marine National Park has been

declared as a National Reserve in 1982 (Uneputty and Evans1997). Since 2006, the Seribu Islands is administrativelydivided into two districts (Estradivari et al. 2007). First,The District of North Seribu Islands which covers 79islands within three sub-districts i.e. Kelapa (36 islands),Harapan (30), and Panggang (13). Second, The District ofSouth 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 ofSeribu Islands relative to Indonesia. The sampling sites indicated by flag.

MADDUPPA et al. – Reef fish diversity linked to environmental gradient 19

districts covering 31 islands. The Seribu Islands MarineNational Park which covers an area of 107.489 ha orapproximately 20% of the total region. Two differentseasons are affecting the Seribu Islands, namely ‘wet’season (November-March) during the northwest monsoon,and ‘dry’ season (May-September) during the southeastmonsoon (Rees et al. 1999). Figure 1 shows the study sitesat Seribu Islands.

The study on reef fish communities was conducted at33 reef sites associated with islands or shoal which wererandomly chosen from each zone along environmentalgradients from the inshore water nearest of Jakarta Bay tothe offshore water of the outer islands and represented eachsub-districts within the archipelago, namely Pari (LancangIs., Bokor Is.), Tidung (Tidung Besar Is., Payung Besar Is.,Karang Beras), Panggang (Karang Bongkok, Gosong Air,Kotok Kecil Is., Karang Congkak, Sekati Is., Semak DaunIs., Air Barat Is., Kotok Besar Is.), Kelapa (Genteng Is.,Jukung Is., Kaliage Besar Is., Kaliage Kecil Is., KayuAngin 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., OpakKecil Is., Sepa Besar Is., Sepa Kecil Is.). Two differentdepths (3 and 10 m) for each sampling site at reef slopewere selected (English et al. 1997).

Data collectionSampling was carried out at each site between 09.00

and 16.30, November 10-20, 2011 during a coral reefexpedition by Marine Biology Laboratory, BogorAgricultural University. Reef fish communities wereassessed by underwater visual census (UVC) on a transectline of 50 meters at each depth (English et al. 1997). In anattempt to reduce daily variability of fish density data(caused by differences in nocturnal and diurnal behavior),sampling excluded the high activity periods of earlymorning and late afternoon (Colton and Alevizon 1981;English et al. 1997). During each census, the observerwaited for 5 to 10 minutes before beginning the datarecording along transect in order to allow the fishes toresume their normal behaviours (Brock 1982; Halford andThompson 1994). Only individuals within 2.5 m on eitherside and 5 m above along the transect, were counted. Eachindividual (cryptic and large pelagic species wereexcluded) was counted and identified to species level. Inorder to avoid the influence of temporal recruitment events,fish recruits up to a size of ~3-5 cm were excluded from thecount. After data collection, reef fish identification wasconfirmed by using standard fish identification books (i.e.Allen 2000; Kuiter 1992). The trophic level for eachspecies was confirmed with the Fishbase (Froese and Pauly2010).

Data analysisThe community Shannon-Wiener diversity index H’

was calculated on a natural logarithm (ln) basis (Magurran1988; Shannon and Weaver 1949). Poisson regressionanalysis was used to test the statistical significance ofdifferences in fish abundance among sites (sub districts), as

well diversity and species richness, using statisticalpackage STATISTICA 7.0.

Multivariate analysis of the fish community data wereconducted using the program PRIMER 5.2.9 (Clarke andGorley 2001; Kruskal 1964). Fish abundance, speciesrichness, and species diversity data were fourth-roottransformed prior to analysis to reduce the influence ofsome overlay abundant species and give more weight torare species while retaining the information value ofrelative abundances, an approach frequently used in themultivariate analysis of community data (Clarke and Green1988; Field et al. 1982).

Bray-Curtis similarity and Non-metric MultidimensionalScaling (MDS) were performed to visualize differences infish communities from the different sites (Kruskal 1964;Shepard 1962). MDS was based on Bray-Curtissimilarities, and 100 restarts were used for the calculations.


A total of 46,263 individual fishes were counted,belonging to 216 species and 29 families (Table 1). A totalof 49 and 78 fish species were recorded from sub-districtsof Pari and Tidung, 109 and 148 from sub-districts ofPanggang and Kelapa, and 106 from sub-district ofHarapan. The values of species richness in this study werealmost similar to that observed by Estradivari et al. (2007)in 2004-2005 in the Seribu Islands (211 species). Inaddition, the species richness of the Seribu Islands werealso similar in range to those observed at other Indonesiancoral reefs, such as Togean Islands and Weh Island (Allenand Werner 2002). The low species richness in the sub-districts of Seribu Islands near from Jakarta Bay (e.g. Pariand Tidung) might be related to the pressures on theenvironment such as bleaching resulting from the 1982/83ENSO event (Brown and Suharsono 1990; Hoeksema1991), and anthropogenic factors such as land-basedcontaminants, man-made objects, oil pollution, domesticand industrial refuse (Willoughby 1986; Uneputty andEvans 1997; Rees et al. 1999).

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

FamilySpecies Trophic

Pari

Tid

ung

Pang

gang

Kel

apa

Har

apan

AcanthuridaeAcanthurus sp. Herbivore 0 1 1 0 0Ctenochaetus striatus Omnivore 0 1 0 4 0ApogonidaeApogon angustatus Carnivore 0 0 0 7 0Apogon apogonides Carnivore 0 0 80 23 0Apogon aureus Carnivore 0 0 11 37 89Apogon cavitienis Carnivore 0 0 20 0 0Apogon chrysopomus Carnivore 0 13 0 0 0Apogon compressus Carnivore 2 20 331 293 192Apogon novemfasciatus Carnivore 0 0 24 0 43Apogon sealei Carnivore 20 0 0 0 0Apogon semiornatus Carnivore 0 0 17 0 2


Archamea fucata Carnivore 0 0 3 0 0Cheilodipterus artus Carnivore 0 0 52 33 88Cheilodipterus isostigmus Carnivore 2 0 0 0 0Cheilodipterus sp. Carnivore 0 0 0 24 0Sphaeramia nematoptera Carnivore 0 0 0 22 0AulostomidaeAulostomus chinensis Carnivore 0 0 0 3 0BalistidaeBalistoides sp. Carnivore 0 1 0 0 0Melichthys indicus Omnivore 0 0 7 0 2CaesionidaeCaesio cuning Planktivore 0 0 429 209 116Caesio teres Planktivore 0 260 372 906 475Pterocaesio digramma Carnivore 0 0 0 0 50Pterocaesio tile Planktivore 0 0 38 80 0CentriscidaeAeoliscus strigatus Carnivore 4 2 0 24 16ChaetodontidaeChaetodon collare Herbivore 1 0 0 0 0Chaetodon meyeri Herbiivore 0 0 5 5 0Chaetodon octofasciatus Coralivore 0 57 131 196 66Chelmon rostratus Coralivore 0 0 3 9 2Chaetodon melanopus Coralivore 0 0 0 0 2Coradion trifasciatus Coralivore 0 0 3 0 6Heniochus chrysostomus Coralivore 0 1 0 0 0Heniochus pleurotaenia Coralivore 0 3 2 0 4Heniochus varius Coralivore 0 0 11 7 1CirrhitidaeParacirrhites sp. Carnivore 1 0 0 0 0DasyatidaeTaeniura lymma Carnivore 0 0 1 1 0EcheneidaeRemora sp. Omnivore 2 0 0 0 0EphippidaePlatax pinnatus Omnivore 0 0 2 0 0Platax teira Omnivore 1 2 2 3 0GobiidaeExyrias belissimus Omnivore 0 0 0 1 0Istigobius decorates Omnivore 0 0 7 8 1HaemulidaePlectorhinchus chaetodontoides Carnivore 0 0 0 2 0Plectorhinchus chrysotaenia Carnivore 0 0 8 0 0Plectorhinchus vittatus Carnivore 0 0 0 2 0HemirhamphidaeHemirhamphus far Omnivore 0 0 1 0 0HolocentridaeMyripristis berndti Carnivore 0 1 0 0 0Myripristis sp. Carnivore 0 0 0 5 0Sargocentron diadema Carnivore 0 0 20 0 0Sargocentron rubrum Carnivore 0 2 0 0 0Sargocentron sp. Carnivore 0 0 0 19 0Sargocentron tiereoides Carnivore 0 0 11 0 0LabridaeAnampses sp. Carnivore 0 0 0 1 0Bodianus mesothorax Carnivore 1 6 19 27 24Cheilinus chlorourus Carnivore 0 0 0 7 0Cheilinus diagramma Carnivore 0 0 0 15 0Cheilinus fasciatus Carnivore 0 29 67 96 19Cheilinus hortulanus Carnivore 0 0 15 8 0Cheilinus oxyrhynchus Carnivore 0 0 0 6 0Cheilinus trilobatus Carnivore 0 0 0 3 0Cheilinus unifasciatus Carnivore 0 0 0 6 0Choerodon anchorago Carnivore 1 10 2 32 0Choerodon fasciatus Carnivore 0 0 4 25 23Cirrhilabrus cyanopleura Planktivore 400 1402 1930 3782 1770Ctenochaetus striatus Omnivore 0 0 7 0 0Diproctacanthus xanthurus Corallivore 1 16 2 27 52Epibulus insidiator Carnivore 0 1 0 6 0Gomphosus varius Carnivore 0 0 0 9 0Halichoeres binotopsis Carnivore 0 5 0 2 1Halichoeres biocellatus Carnivore 0 0 18 39 19Halichoeres chloropterus Carnivore 0 0 45 30 0Halichoeres chrysotaenia Carnivore 0 5 7 21 0Halichoeres dussumieri Omnivore 0 0 21 0 53Halichoeres hortulanus Carnivore 3 17 29 80 20

Halichoeres leucurus Omnivore 4 13 45 58 39Halichoeres marginatus Omnivore 0 4 15 41 22Halichoeres melanochir Omnivore 0 0 28 48 5Halichoeres melanurus Omnivore 3 11 67 47 29Halichoeres nigrescens Carnivore 14 2 2 1 0Halichoeres ornatissimus Carnivore 0 0 12 30 0Halichoeres richmondi Carnivore 0 9 28 22 11Halichoeres scapularis Carnivore 1 0 0 0 0Halichoeres sp. Omnivore 6 8 74 8 1Halichoeres vrolikii Omnivore 5 0 0 1 0Hemigymnus melapterus Carnivore 3 4 10 26 4Labroides chrysotaenia Omnivore 0 0 0 0 2Labroides dimidiatus Carnivore 6 16 44 61 27Macropharyngodon negrosensis Omnivore 0 0 2 7 8Neoglyphidodon melas Omnivore 0 0 0 0 0Pseudocheilinus hexataenia Omnivore 0 0 5 7 11Pseudojuloides cerasinus Omnivore 0 0 18 0 18Pteragogus amboinensis Omnivore 0 0 0 0 22Stethojulis trilineata Omnivore 0 11 0 0 3Thalassoma lunare Omnivore 24 78 132 195 45Thalassoma lutescens Omnivore 0 2 0 0 5Thalassoma purpureum Carnivore 0 0 11 7 22Thalassoma quinquevittatum Carnivore 0 0 16 0 19LethrinidaeLethrinus erythropterus Carnivore 0 0 0 12 0LutjanidaeLutjanus biguttatus Carnivore 0 2 4 26 0Lutjanus decussatus Carnivore 0 6 25 25 3Lutjanus kasmira Omnivore 0 0 0 6 0Lutjanus russellii Carnivore 0 0 0 4 0MullidaeParupeneus barberinus Carnivore 0 0 0 5 0MuraenidaeGymnothorax javanicus Carnivore 0 0 0 1 0NemipteridaePentapodus caninus Carnivore 0 0 46 28 28Pentapodus sp. Carnivore 0 0 0 1 0Pentapodus vitta Carnivore 0 0 0 18 0Scolopsis bilineatus Carnivore 3 22 29 50 17Scolopsis ciliatus Carnivore 0 3 0 9 0Scolopsis lineatus Carnivore 0 0 17 14 17Scolopsis margaritifer Carnivore 0 6 0 41 0Scolopsis sp. Carnivore 0 0 0 4 0Scolopsis temporalis Carnivore 1 0 0 0 0Scolopsis trilineatus Carnivore 1 0 0 26 12PempheridaePempheris oualensis Carnivore 0 0 0 15 36Pempheris sp. Carnivore 50 0 0 0 0PomacanthidaeCentropyge vrolikii Herbivore 0 1 0 0 0Chaetodontoplus mesoleucus Herbivore 0 19 57 199 69Pomacanthus sextriatus Herbivore 0 0 2 0 0PomacentridaeAbudefduf bengalensis Omnivore 0 0 0 91 25Abudefduf curacao Omnivore 0 0 0 18 0Abudefduf septemfasciatus Omnivore 3 0 19 0 0Abudefduf sexfasciatus Omnivore 0 111 107 204 121Abudefduf sordidus Omnivore 0 0 49 0 0Abudefduf vaigiensis Omnivore 0 94 119 139 61Acanthochromis polyancanthus Omnivore 0 0 0 11 13Amblyglyphidodon aureus Omnivore 0 2 0 25 2Amblyglyphidodon batunai Omnivore 0 0 49 79 87Amblyglyphidodon curacao Omnivore 20 114 519 560 451Amblyglyphidodon leucogaster Omnivore 0 16 226 342 163Amblyglyphidodon nigroris Omnivore 0 39 0 0 0Amphiprion akallopisos Omnivore 2 0 2 12 0Amphiprion akindinos Omnivore 0 0 0 0 5Amphiprion clarkii Omnivore 0 0 0 3 3Amphiprion ocellaris Omnivore 0 0 0 0 6Amphiprion perideraion Omnivore 0 0 0 0 2Amphiprion sandaricinos Omnivore 0 0 0 0 4Cheiloprion labiatus Omnivore 0 0 0 3 0Chlororus sordidus Omnivore 0 0 0 2 0Chromis amboinensis Omnivore 0 90 50 93 94Chromis atripectoralis Omnivore 0 39 708 500 878


Chromis fumea Planktivore 80 0 0 50 303Chromis nitida Omnivore 0 0 0 5 0Chromis scotochilopterus Planktivore 0 0 24 0 34Chromis smithi Omnivore 0 0 0 17 0Chromis ternatensis Planktivore 14 52 2 926 712Chromis viridis Omnivore 0 142 159 372 177Chromis xanthura Planktivore 0 0 69 78 70Chrysiptera cyanea Omnivore 0 0 10 0 0Chrysiptera hemicyanea Omnivore 0 0 21 21 9Chrysiptera parasema Planktivore 0 0 30 22 32Chrysiptera sp. Omnivore 6 0 0 0 0Dascyllus melanurus Omnivore 0 0 0 1 0Dascyllus reticulatus Omnivore 0 0 0 1 0Dascyllus trimaculatus Omnivore 0 1 0 80 10Diproctacanthus xanthurus Corallivore 0 1 0 2 0Dischistodus melanotus Herbivore 0 0 47 48 35Dischistodus perspicillatus Herbivore 0 0 0 10 0Dischistodus prosopotaenia Herbivore 0 24 64 101 32Hemiglyphidodon plagiometopon Herbivore 0 0 3 24 5Neoglyphidodon bonang Omnivore 0 0 2 0 0Neoglyphidodon crossi Omnivore 0 25 167 58 94Neoglyphidodon leucogaster Carnivore 0 25 0 0 0Neoglyphidodon melas Omnivore 2 19 27 111 117Neoglyphidodon nigroris Omnivore 3 18 37 129 17Neoglyphidodon thoracotaeniatus Omnivore 0 0 0 88 0Neopomacentrus anabatoides Planktivore 0 0 0 38 0Neopomacentrus bankieri Carnivore 0 0 0 0 20Neopomacentrus cyanomos Carnivore 0 0 0 156 0Neopomacentrus filamentosus Planktivore 0 0 120 178 71Pomacentrus alexanderae Omnivore 1 1338 2320 4058 1335Pomacentrus amboinensis Omnivore 0 0 0 57 0Pomacentrus brachialis Omnivore 6 0 0 0 0Pomacentrus burroughi Herbivore 1 22 23 77 5Pomacentrus coelestis Omnivore 0 0 56 0 12Pomacentrus cuneatus Omnivore 7 0 0 0 0Pomacentrus javanicus Omnivore 0 14 0 0 0Pomacentrus lepidogenys Planktivore 13 33 33 514 98Pomacentrus littoralis Omnivore 0 18 0 0 0Pomacentrus milleri Omnivore 5 14 0 56 11Pomacentrus moluccensis Omnivore 5 306 378 297 103Pomacentrus simsiang Omnivore 0 0 0 16 0Pomacentrus smithi Omnivore 50 657 775 2760 239Pomacentrus sp. Omnivore 5 1 0 9 2Pomacentrus xanthosternus Omnivore 0 12 0 0 0Premnas biaculatus Omnivore 1 0 0 2 0Pristotis obtusirostris Omnivore 0 0 18 0 23ScaridaeChlorurus bleekeri Herbivore 0 0 1 18 0Chlorurus microrhinos Herbivore 0 0 8 29 0Chlorurus sordidus Omnivore 0 9 33 107 39Scarus chameleon Herbivore 0 0 0 0 4Scarus dimidiatus Herbivore 0 0 6 0 21Scarus flavipectoralis Herbivore 0 0 6 0 18Scarus frenatus Herbivore 0 0 5 0 10Scarus ghobban Herbivore 0 0 2 17 1Scarus globiceps Herbivore 0 2 5 7 18Scarus niger Herbivore 2 7 27 37 5Scarus quoyi Herbivore 0 8 8 8 0Scarus rivulatus Herbivore 0 42 17 35 13Scarus sordidus Herbivore 0 0 0 5 0Scarus sp. Herbivore 2 26 0 11 1Scarus xanthopleura Herbivore 0 0 0 5 0ScorpaenidaePterois volitans Carnivore 0 0 0 1 0SerranidaeCephalopholis argus Carnivore 0 0 0 26 0Cephalopholis boenak Carnivore 4 1 0 13 0Cephalopholis microprion Carnivore 1 4 4 16 2Cephalopholis sp. Carnivore 1 0 0 1 0Diploprion bifasciatum Carnivore 0 1 0 0 0Epinephelus fasciatus Carnivore 0 0 0 1 0Epinephelus merra Carnivore 0 0 0 2 0Epinephelus rivulatus Carnivore 0 0 7 6 6Epinephelus sexfasciatus Carnivore 0 0 5 1 4

SiganidaeSiganus argenteus Herbivore 0 0 0 0 1Siganus canaliculatus Herbivore 0 7 0 0 0Siganus guttatus Herbivore 0 0 0 12 0Siganus virgatus Herbivore 0 3 0 16 0Siganus vulpinus Herbivore 0 3 0 0 0ZanclidaeZanclus cornotus Herbivore 0 0 0 2 0

The composition of the five most diverse fish familiesthat were observed in all sub-districts are given in Table 2.The most abundant families at sub district of Pari wereLabridae (wrasses), followed by Pomacentridae (dam-selfishes). The most abundant families at the rest sub-districts were Pomacentridae (damselfishes), followed bythe Labridae (wrasses). Overall, the most diverse familiesin the reef community were Pomacentridae and Labridae.This pattern was also observed in the previous study at theislands (Estradivari et al. 2007), and at other locations inIndonesia (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 3.0 - 5.0 2.2 4.5Caesionidae - 4.8 7.8 6.0 6.4Chaetodontidae - 1.1 1.4 - -Labridae 59.8 30.5 24.7 23.9 24.8Nemipteridae 0.6 - - - -Pempheridae 6.3 - - - -Pomacentridae 28.4 59.6 57.6 62.2 59.7Scaridae - 1.7 - 1.4 1.4

The Shannon-Wiener diversity indices of the fishcommunities, the average species richness and the averagefish abundance are shown in Figure 2. The sub-district Parias the nearest to Jakarta Bay, had the lowest fishabundance, species richness, fish diversity, while the sub-district Harapan as the outlier islands had the highest ones.The fish abundance ranged from 265 ± 140 (sub-district ofPari) 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 from20 ± 7 (Pari) to 36 ± 5 species/250m2 (Harapan) over theentire study period. The pattern showed that values on thefish abundance, diversity index and species richnessincrease toward north of Seribu Islands. The highabundance and species richness might be related to livecoral coverage. The nearest region to Jakarta Bay haslowest live coral coverage and the live coral coverageincrease toward to the north of the islands (Estradivari et al.2007). In the present study, the sub-district’s reefs did havea significant influence on fish abundance and speciesrichness, but not for diversity index (Table 3). Multiplestudies have reported a positive correlation with thestructural complexity of a coral reef habitat for fishabundance (e.g. Walker et al. 2009), species richness (e.g.Wilson et al. 2007), and species diversity (e.g. Öhman andRajasuriya 1998).


Table 3 Results of Poisson regression for abundance, speciesrichness, and diversity of fish assemblages (*<0.001, n.s. notsignificant)

Variable Factor df W.S p

Abundance Site 4 1868.0 0.00 *Species richness Site 4 21.083 0.00 *Shannon-Wiener index (H') Site 4 0.50872 0.97 n.s

Figure 2. The average values of (a) fish abundance, (b) speciesrichness, and (c) species diversity (Shannon-Wiener Index; lnbasis) of fish assemblages at the sampling sites. The arrow showsthe direction from Jakarta Bay to the offshore water of the outerislands.

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

by omnivorous and carnivorous fishes. Even though thereis a strong correlation between coral and fish, only few ofthe species found in a coral reef ecosystem dependspecifically on scleractinian corals (Munday et al. 2007). Astudy indicated that the fish communities were likely notstructured by habitat-mediated factors such as predationimpact or available space, but different factors such asrecruitment or migration were playing a stronger role(Madduppa et al. 2012). However, no significantdifferences in diversity indices were found among the sub-districts (Table 3). This might be explained by feedingspecialization among coral fishes. The specialization infood can reduce competition within a reef (Gladfelter andJohnson 1983; Ross 1986), and increase species diversity.A study found that some species such as scarids appearedin only specific habitat which had the lowest amount of livecoral but the highest amount of dead coral and algae(Madduppa et al. 2012). Other species such as Chaetodontshave been observed to appear on high percentage of livecoral which they use for food or shelter (Cox 1994).

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

The multivariate analysis of fish abundance, speciesrichness and fish diversity were done using the Bray Curtissimilarity index and non-metric multidimensional scaling(MDS). The MDS plot and Bray-Curtis similarity havedistinctly clustered the sub-districts from southern andtoward north of the Seribu Islands based on fish abundance,species richness and fish diversity. The results showed thatthe sub-districts can be clustered into 3 groups based onfish abundance, with 0 stress value (Figure 4). Group oneconsists of one sub-district (Pari) located in the southernpart of the Seribu Islands near Jakarta Bay. Group twoconsists of three sub-districts (Tidung, Panggang, andKelapa) located in mid of the archipelago. The third groupconsists of one sub-district (Harapan) located in thenorthern part of the Seribu Islands. The species richnessand fish diversity indices showed that the sub-districts canbe clustered into two groups (1=Pari and Tidung, 2=Panggang Kelapa, Harapan). These figures showed that theislands within archipelago seemed to be linked to theenvironmental factors such sedimentation, pollution andother human activities in Jakarta Bay and Seribu Islands(Rees et al. 1999; Rachello-Dolmen and Cleary 2007;Willoughby 1986).

Sub-district of the Seribu Islands


Figure 4. Dendogram based on Bray-curtis similarity (left) and MDS plot (right) of fish communities at the Seribu Islands, showingpattern 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 eachstudied reefs, the present study results showed that thebiodiversity of reef fishes across the Seribu Islands seemsto be linked to environmental condition such as turbidityand level of pollution from Jakarta Bay toward the northernof the islands. Further studies of reef fish communities andhabitat characteristics throughout the region are needed todocument environmental changes over time.

ACKNOWLEDGEMENTS

We wish to thank the following institutions and peoplefor their assistance and help during this study. MarineBiological Laboratory, Bogor Agricultural University (IPB)Bogor for the logistic support, members of FisheriesDiving Club, Bogor Agricultural University (IPB) Bogorfor all their help in the field work. The study was supported

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

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Variability of soil physical indicators imposed by beech and hornbeamindividual trees in a local scale

YAHYA KOOCH1,♥, SEYED MOHSEN HOSSEINI1, SEYED MOHAMMAD HOJJATI2, ASGHAR FALLAH2

1Department 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, email: [email protected]

2Department 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 individualtrees in a local scale. Biodiversitas 14: 25-30. The objective of our study was to determine if soil physical indicators could be related tothe influence of the individual trees in stands of mixed species growing on steep slopes in the Hyrcanian forests of Iran. Research wasconducted in a forest dominated by beech (Fagus orientalis Lipsky) and hornbeam (Carpinus betulus L.) interspread with the otherdeciduous tree species. Due to, twenty hectare areas of Experimental Forest Station of Tarbiat Modares University was considered innorthern 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 soilsampling from every tree species and diameter class as three replications. All of soil samples were excavated in north aspect and at thenearest point to tree collar for more precision. Soil samples were taken at 0-15, 15-30 and 30-45cm depths using auger soil sampler with81cm2 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 foundamong 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 anysignificant difference. Current research has shown that the influence of individual trees with different diameter classes can be detected inforest floors and upper minerals soil layers even under mixed stands in steepy sloping landscapes. This subject should be considered innatural forests management.

Key words: Bulk density, Hyrcanian forest, moisture, old trees, soil texture

INTRODUCTION

Tree-soil interactions and their influence on tree fitnessand forest community dynamics are complex. Many currenttheories on spatial heterogeneity and species diversity offorest communities are based on the premise that speciesinteraction is controlled by competition for resources suchas light, water, nutrients (Binkley and Menyailo 2005).Although these resources are largely constrained by thephysical environment, the influence of canopy trees onresources can be of significant importance in forestecosystem dynamics. This biotic control over resources hasreceived little attention until recently in understandingforest ecosystem dynamics. Several authors havedemonstrated the existence of a close interaction betweenplant and soil (Lovett et al. 2002; Compton et al. 2003;Templer et al. 2005). The evidence above suggests thattree-soil feedbacks need to be incorporated into the conceptof species diversity and spatial heterogeneity in forestecosystems in order to gain more insight in long-termforest dynamics. The soil under the influence of a forestdevelops properties that vary spatially with relation to thelocation of the trees. This variation in soil properties isfrequently reflected in the distribution of the various

species of the ground flora. The amelioration ordegradation of the forest soil takes place with each tree as acenter of influence (Kooch et al. 2011). Individual speciesare an important control on soil properties such asstructure, water availability, and biota, as well as nutrientcycling. Tree species may influence soil nutrient cyclingdirectly, via nutrient uptake (Turner et al. 1993), litterinputs (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 andfaunal activities (Smolander and Kitunen 2002).

Studies of trees grown in monocultures effectivelyisolate species effects on soils, but may not adequatelycapture species effects in mixed stands (Rothe and Binkley2001). Despite continued research into tree species effectson soil nutrient cycles, the generality of these effectsremains unknown (Binkley and Menyailo 2005). Forexample, leaf litter decomposition experiments have shownthat mixtures of litter of different species can exhibitadditive, neutral, and antagonistic effects on overalldecomposition that are not easily predicted from thecharacteristics of the individual litters alone (Gartner andCardon 2004). More generally, experimental studies of


grasslands have shown that species diversity and functionalcharacteristics can impact a range of ecosystem processesthat serve as the context for individual species effects onsoils (Tilman et al. 2001). Thus, plants can shape long-termpatterns of soil and ecosystem development (Jenny 1941)in ways that may affect subsequent interspecificinteractions and plant-soil relationships. Old-growth forestsof northern Iran provide a unique opportunity to examinetree species-soils relationships in a wide range of mixed-species ecosystems that developed with minimalanthropogenic disturbance. Northern forests of Iran stretchup to an altitude of 2800 m asl. and comprise differentforest types with 80 species of trees and shrubs. There is1.9×106 ha of hardwood forests in the north of Iran, whichis called Hyrcanian ecosystem (Hosseini et al. 2007;Rouhi-Moghaddam et al. 2008; Poorbabaei and Poorrostam2009). The Hyrcanian forests are one of the last remnantsof natural deciduous forests in the world (Sagheb Talebi2000).

Beech (Fagus orientalis Lipsky) is one of the mostimportant elements of forests in the temperate broad-leafforest biome and represents an outstanding example of there-colonization and development of terrestrial ecosystemsand communities after the last ice age, a process which isstill ongoing (Mosadegh 2000; Marvie Mohadjer 2007). Inthe north of Iran, pure and mixed oriental beech forestscover 17.6 per cent of the surface land area and represent30 per cent of the standing volume. Beech is the mostvaluable wood-producing species in the Caspian forests(Resaneh et al. 2001). The beech trees are found in smallgroups up to 500m asl. while individuals have beenreported from 110m up to 2650m. At low altitudes, theyoccur mixed with hornbeam (Carpinus betulus L.) (Marvie

Mohadjer 2007). In spite the important of Hyrcanianforests, but earlier study that has evaluated the effects ofdominated individual trees on soil characters at the standlevel wasn't considered. The objective of this study is toquantify the effects of beech and hornbeam single treespecies on soil physical indicators in an old-growthhardwood forest of Iran that is the first survey in theseforests.


Site descriptionThis research was conducted in Experimental Forest

Station of Tarbiat Modares University located in atemperate forest of Mazandaran province in the north ofIran, between 36˚ 31’ 56˝ N and 36˚ 32‘ 11˝ N latitudesand 51˚ 47‘ 49˝ E and 51˚ 47‘ 56˝ E longitudes (Figure 1).The maximum elevation is 1700m and the minimum is100m. Minimum temperature in December (6.6˚C) and thehighest temperature in June (25˚C) are recorded,respectively. Mean annual precipitation of the study areawere from 280.4 to 37.4 mm at the Noushahr citymetrological station, which is 10Km far from the studyarea. For performing this research, a limited area of reserveparcel (relatively undisturbed) considered that was coveredby Fagus orientalis and Carpinus betulus dominant stands.This limitation had an inclination 60-70 percent withnortheast exposure at 546-648 m asl. Bedrock is limestone-dolomite with silty-clay-loam soil texture. Presence oflogged and bare roots of trees is indicating rootingrestrictions and soil heavy texture (Kooch et al. 2010).

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

Islamic Republic of Iran

Experimental Forest Station ofTabiat Modares University

KOOCH et al. – Soil characteristics of beech and hornbeam trees habitat 27

Soil samplingDue to examine the influence of forest individual trees

on soil physical indicators, twenty hectare areas ofExperimental Forest Station of Tarbiat Modares Universitywas considered. The positions of trees with diameter atbreast height (DBH) (1.3 m) more than 45 cm (Goodburnand Lorimer 1999; Scahrenbroch and Bockheim 2007;Kooch et al. 2011) were recorded by Geographical PositionSystem (GPS). Three single-trees (was defined as treeswith canopy cover separated from other trees and covereddistinguished space) considered for soil sampling fromevery tree species and diameter class as three replications.All of soil samples were excavated in north aspect and atthe nearest point to tree collar for more precision. Soilsamples were taken at 0-15, 15-30 and 30-45cm depthsusing auger soil sampler with 81cm2 cross section (Koochet al. 2011).

Laboratory analysesFor this purpose, large live plant material (root and

shoots) and pebbles in each sample were separated by handand discarded. The air-dried soil samples were sieved(aggregates were crushed to pass through a 2 mm sieve) toremove roots prior to analysis. Bulk density at air driedmoisture content was measured by Plaster (1985) method(clod method). Soil texture was determined by theBouyoucos hydrometer method (Bouyoucos 1962). Soilmoisture was measured by drying soil samples at 105° Cfor 24 hours (Ghazanshahi 1997).

Statistical analysesNormality of the variables was checked by Kolmogrov-

Smirnov test and Levene test was used to examine theequality of the variances. Differences between diameterclasses and depths in soil properties were tested with two-way analysis (ANOVA) using GLM procedure, withdiameter classes (45-55, 55-65, 65-75, 75-85, 85-95, 95-105cm) and depth (0-15, 15-30 and 30-45 cm) asindependent factor. Interactions between independentfactors were tested also. Duncan test was used to separatethe averages of the dependent variables which were

significantly affected by treatment. Independent sample t-test carried out for compare means of soil propertiesbetween beech and hornbeam single trees. Significantdifferences among treatment averages for differentparameters were tested at P ≤ 0.05. SPSS v. 11.5 softwarewas used for all the statistical analysis.


Analysis of variance of studied characters is indicatingthat in relation to beech single trees, the greater amounts ofbulk density belong to 45-55cm diameter class and the leastwas detected in 65-75cm class (Table 1). This charactershowed the maximum and minimum in 45-55cm and 75-85cm diameter classes, respectively under hornbeam trees(Table 2). Bulk density was significantly greater underbeech than under hornbeam (Figure 2). This character tendsto be less in 0-15cm depth than in 15-30cm and 30-45cmdepths (Tables 1 and 2). Soil texture components showedno significantly difference among diameter classes ofbeech trees, but the greater amounts of silt content wasfound in 30-45cm depth (Table 1). Under hornbeam, thehigher values of silt, clay and lower amounts of sand wereconsidered in 75-85 diameter class (Table 2). Sand contentwas significantly higher in 0-15cm, whereas the greateramounts of silt detected in 30-45cm depth. Clay amountsdid not show any significant difference between depths(Table 2). Silt and clay were significantly greater underhornbeam than under beech (Figure 2). Moisture wassignificantly higher under beech than under hornbeam(Figure 2), whereas soil depths and diameter classes did notshow any significant difference (Tables 1 and 2).

Results of present research are indicating that individualtrees can be effective on soil physical indicators. Theweight of a tree, combined with the movement of structuralroots during windy conditions, can compress soils overcentimeter-scales (Chappell et al. 1996). With consideringto mountainous position of Hyrcanian forests in Iran andpresence 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 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)

Diameter class (cm)

F-value 7.60** 0.70ns 2.14ns 0.02ns 2.23ns0-15 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

Soil depth (cm)

Interaction 0.70ns 0.09ns 0.38ns 0.00ns 0.77nsNote: ** Different is significant at the 0.01 level. (ns): Non significant differences (P > 0.05). Values are the means ±St. error of themean (in parenthesis). Within the same column the means followed by different letters are statistically different (P < 0.05).


Table 2. Mean of soil physical indicators in relation to diameter classes and soil depth in hornbeam site

Variable / soil character Bulk density (g/cm3) 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)

Diameter class (cm)

F-value 13.89** 17.08** 24.79** 11.10** 0.70ns0-15 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

Soil depth (cm)

Interaction 0.35ns 3.95** 16.39** 0.00ns 0.27nsNote: ** 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 arestatistically different (P < 0.05).

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

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

density increased in soil deeper layers. Both living anddecayed roots can create well-connected pores in thetopsoil 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 todecreasing of bulk density, finally. Bulk density showedsignificantly increasing under beech than hornbeam.

Soil acidification due to an increase in the rate ofdissolution of soil minerals beneath trees (Augusto et al.2000), acidic litter-fall (Chappell et al. 2006) or acidicexudates (Chappell et al. 2007) has been shown to reducesoil structural stability. This reduced stability can lead to areduction in soil porosity. High rates of leaching byinfiltrating stem-flow can exacerbate the acidificationeffect (Augusto et al. 2002). Regarding to low acid under

1.09

1.1

1.11

1.12

1.13

Beech Hornbeam

Bul

k de

nsity

(gr/

cm3)

b

at = 2.93

Sig = 0.00

29.530

30.531

31.532

32.533

Beech Hornbeam

San

d (%

) a

b

t = 3.34Sig = 0.00

37.5

38

38.5

39

39.5

40

Beech Hornbeam

Silt

(%)

b

a

t = - 2.68Sig = 0.00

28.5

29

29.5

30

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Cla

y (%

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3939.239.439.639.8

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Moi

stur

e (%

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a

b

t = 2.22Sig = 0.00

KOOCH et al. – Soil characteristics of beech and hornbeam trees habitat 29

beech than hornbeam, thus instability is more considered insoils imposed by beech trees. By this reason, porosity isdecreased under beech and bulk density will be increasedthat is according to obtained result in this research. The soilacidity also affects the presence and abundance of soilfauna, such as earthworms (Neirynck et al. 2000). Asearthworm activity creates more stable soil aggregates andadds macro-porosity, reduced abundance would beexpected to increase of bulk density. In general, soil pHdetected as the most important effective factor onearthworms abundance (Boettcher and Kalisz 1991;Neirynck et al. 2000). Research results of Kooch et al.(2011) in study area showed that soil pH was significantlyless under beech than hornbeam and earthworm'sabundance were fewer also. Thus bulk density showedsignificantly increasing under beech than hornbeam. Thisresult also can be related to more activity of earthworm'spopulation under hornbeam individual trees. Thecomposition of the over story has an impact on soilstructure (Read and Walker 1950). Graham and Wood(1991), Graham et al. (1995) have shown that the soilstructure and its stability were tree species dependent,probably because of differential effects on worm activity.

Furthermore, wild and domesticated animals useisolated trees for shelter during rainstorms or for shadefrom intense solar radiation. This congregation of animals,particularly at times when the soil is wet, can compact thesoil and thereby increase the bulk density of the soilhorizon (Drewry et al. 2000). Regarding to more amountsof moisture under beech than hornbeam, soil compactionwas more occurred, thus increasing of bulk density is moreconsidered. Silt and clay were more gathered underhornbeam than beech that can be related to earthworm'sgreater densities as with creation of macropores they aredue to changes in the components of soil texture.Earthworms are able to transferring of smaller componentsof soil (i.e. clay and silt) to different layers. Beechindividual trees with superficial rooting system have moreability for preservation of soil moisture in upper soil. Thus,moisture was significantly higher under beech than underhornbeam, whereas soil depths did not show any significantdifference. In total, compared to open areas, the reducedprecipitation received beneath tree canopies due toenhanced wet-canopy evaporation (David et al. 2006)combined with greater root abstraction to supporttranspiration can lead to considerably greater topsoil dryingduring rain-free periods (Ziemer 1968; Katul et al. 1997).

The study has shown that the influence of individualtrees with different diameter classes can be detected inforest floors and upper minerals soil layers even undermixed stands in steepy sloping landscapes. The magnitudeof the differences observed depends to some degree on thenature of the forest stand and under story vegetation and onclimatically and topographically controlled processes suchas litter redistribution and soil creep. In any case, the soillandscape may be viewed as a mosaic, with properties ofthe individual pedons composing the mosaic reflecting theoccurrence and physical characteristics of the tree speciespresent. Differences in substrate properties beneath thecrown of juxtaposed tree species may in some cases be

large enough to result in short-range variations in soilproperties and plant growth (Kooch et al. 2011). Presentresearch was the first survey to quantify the local effect ofindividual trees on soil physical indicators in Hyrcanianforests of Iran. However, the effect of over story species isstrongly influenced by forest management (e.g. low densitystands or mixed stands) that, further researches shouldaddress this point.

CONCLUSION

The forest soils can be strongly influenced by treespecies. Many studies have addressed the effects ofmonocultures on forest soil physical, but few haveexamined the effects of varying ratios of species withinstands. In current research, the validity of the concept of"single-tree influence circles" was tested in a forestdominated by beech (Fagus orientalis Lipsky) andhornbeam (Carpinus betulus L.) on steep slopes in theAlborz Mountain, Hyrcanian forest of Iran. In this paper,we presented data on and discussed the effects ofindividual species trees on soil physical indicators in asingle soil map unit in an old-growth northern hardwoodforest. Soil bulk density and moisture were significantlygreater under beech than under hornbeam. Whereas, siltand clay were significantly greater under hornbeam thanunder beech. We propose that soil diversity in this old-growth northern hardwood forest is substantial and suggestthat it be considered in soil survey and forest management.

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Species composition of understory vegetation in coal mined land inCentral Bengkulu, Indonesia

WIRYONO♥, ARIF BUHA SIAHAANDepartment of Forestry, Faculty of Agriculture, University of Bengkulu. Jl. Raya Kandang Limun, Bengkulu 38371A, Bengkulu, Indonesia.

Tel.: +62-736-21170; Fax.: +62-736-21290; email: [email protected].

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 minedland is done by revegetating the land. In addition to planted species, pioneer species usually grow naturally in mined land. Theobjectives of this study were to know the species composition of understory vegetation growing naturally in coal mined land plantedwith Gmelina arborea in Central Bengkulu, Indonesia, and to compare that composition with that of unreclaimed coal mined land and ofnatural forests. Data were collected by sampling understory vegetation in study site. Each plant was identified, harvested and oven-driedto find the biomass. Results showed that the reclaimed mined land had 16 understory species from 6 families, and the abandoned minedland had 10 species from 3 families, lower than that of natural forests, which were 92 and 112. The three most important species wereScleria sumatrensis Retz, Eragrostis chariis (Schult.) Hitchc and Paspalum conjugatum Berg. The species composition of understoryvegetation in reclaimed mined land had high similarity with that of abandoned mined land but was totally different from that of naturalforests.

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 inIndonesia has destroyed the natural forest and createdbarren land. In general, mined soils have physical,chemical and biological problems that may inhibit optimalplant growth (Bradshaw 1997; Lottermoser 2010). The useof heavy machinery and the high content of rock haveresulted in highly compacted soil material, impeding rootpenetration (Bussler et al. 1984). Chemically, many minedlands 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 toovercome this low fertility. Physically, soil compaction canbe reduced by ripping, tilling, or contouring to improveaeration and infiltration (Ashby 1997; Jacinthe and Lal2007). Chemically, soil acidity is alleviated by liming(Bradshaw 1997). Biologically, mined land may beintroduced with mycorrhiza (Cordell et al. 1999),Rhizobium (Widyati 2007) or earthworms (Vimmerstedtand Finey 1973; Nurliana and Wiryono 2004).

Naturally, succession will bring back the compositionof vegetation of mined land into its original one, but ittakes very long time. In Western Australia, Norman et al.(2006) found that vegetation composition of mined landhad not reached the original state after it had been

revegetated for 14 years. Chaffey and Grant (2000) foundsimilar situation in Tomago, New South Wales, Australia.Previous studies in North America also showed the slowprocess of succession in mined land (Glen-Lewin 1979;Jonescu 1979).

To speed up the succession, deliberate restorations ofmined land have been done. Restoration of degraded landmay be viewed as reconstruction of original ecosystem(Cooke and Johnson 2002), but there is an argumentwhether this is desirable or possible due to the dynamicnature of ecosystem and the irrevesibility of some changesthat might have happened (Hobbs and Harris 2001).Revegetation of mined land is an early step to bring backthe original ecosystem. However, due to the low soilfertility of the land, the species planted are usually thepioneer ones which can grow in harsh condition. InSumatra, several pioneer species have been successfullyplanted in mined land such as Paraserianthes falcataria,Leucaena leucocephala, Sesbania grandiflora, and Acaciamangium (Munawar 2003; Nurliana and Wiryono 2004;Suhartoyo et al. 2012). Several pioneer shrub species havebeen used to improve soil chemical, physical and biologicalproperties of mined land in Bengkulu (Prawito 2009).Litter from pioneer vegetation can improve soil nutrient forplants in mined land (Munawar et al. 2011).

In addition to planted species, some pioneer speciesnaturally invade the area. Both the planted and naturallyinvading species will undergo succession and the


community will finally reach the climax. Communitystructure and species composition are some factors to beconsidered in determining the success of ecosystemrestoration (Tongway and Ludwig 2006; Cooke andJohnson 2002). The objectives of this research were toknow the species composition of understory (Br: under-storey) plants growing naturally in coal mined land recentlyrevegetated with Gmelina arborea in Central Bengkulu,Indonesia, and to compare it with that of abandoned orunrevegetated coal mined land and of natural forests.


Site and timeThis 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 usedto be hill forest in the Bukit Barisan Mountain range, withaltitudes of 300-500 m above sea level. It has wet climatewith an average annual rainfall approximately 3,000 mm.

SamplingSamplings of ground cover vegetation and soil were

done in two types of mined lands, namely the reclaimedland planted with Gmelina arborea 1.5 years before thesampling and one abandoned (un-reclaimed) mined land.The reclaimed mined land was introduced with mycorrhiza

and Rhizobium by another researcher. This revegetatedland consisted of two sites having different soil colors. Thefirst site was strong brown (7.5 YR 4/6 in Munsell soilcolor charts) and the other was black (5Y 2.5/1). Theabandoned land had dark yellowish brown (10 YR ¾) soilmaterials. We did not investigate the cause of colordifferences among sites.

Samplings of vegetation were done in 1 x 1 m plotswith 25% sampling intensity. The number of sample plotsin strong brown reclaimed soils was 63, in black reclaimedsoil 72 and in abandoned mined soil 135. The plots wereplaced systematically with random start.

For every plot, each species of understory plantsconsisting of herbs and shrubs less than 2 m in height wererecorded, harvested and placed in paper bags. Harvestmethod was used because this method can give betterquantitative data than percent coverage method. The bagswere then oven-dried at a temperature of 105o C for 24hours or more until the weight was constant. Foridentification, a specimen of herbarium was taken for eachspecies. These specimens were oven-dried at a temperatureof 80 o C for 8 hours.

A composite soil sample was taken from each landtype. The soil samples were then dried and taken to SoilLaboratory in the Faculty of Agriculture, the University ofBengkulu, for chemical and physical analyses. Chemicalanalyses were done to find out the pH, and nitrogen,phosphor, and potassium content. Physical analyses weredone 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 33

Data analysesPlant species identification was conducted in the

Herbarium of Forestry Department, University ofBengkulu, using several field guides (Soerjani et al. 1987;Sastrapradja and Afriastini 1980, 1981; Hafliger andScholz 1980, 1981; Hafliger et al. 1982).

Species importance was determined by biomass,because clumped grasses and creeping plants constituted alarge portion of understory plants in the study site. It is notpossible to count individual stem of grasses in clumps andof creeping plants. According to Whittaker (1975) speciesimportance in a community can be determined by severalquantitative measurements, one of which is biomass. Thisstudy did not use percent coverage method, because visualestimate of coverage would give less accurate data thanactual weighing of the biomass.

Biomass for each plant, calculated using the formula inBrower et al. (1998):

Bi =A

Wi

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, SørensenIndex of Similarity was calculated (Mueller-Dombois andEllenberg 1974).

Sørensen Index:

ISS =BA

c

2 x 100 %

A = the number of all species found in in A communityB = the number of all species found in B communityc = the number of common species (found in both A

and B)

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


Species compositionThe understory vegetation in mined land was composed

of 17 species, from 7 families. The black reclaimed soil hadthe highest number of species, 16, while the dark brownreclaimed soil had only 11 species, almost the same withthe non reclaimed land which had 10 species (Table 1;Figure 2). The number of species in this mined land washigher than 4-year old vegetation in another mined inMuara Enim, South Sumatra, which was only 10(Suhartoyo et al. 2012). The species richness of this mined

land was much lower than those in natural forests inBengkulu, 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 notdetermined because it is not possible to count the numberof plants of clumped grasses and creeping plants. Numberof species is the simplest measurement of species diversity(Whittaker, 1975). Colinvaux (1986) even believed thatnumber of species is more meaningful than diversity index.

Table 1. Species composition of understory vegetation in coalmined land of Danau Mas Hitam Company in Taba PenanjungSub District, Central Bengkulu District.

Species Family A1 A2 B

Chromolaena odorata (L.)R.M.King & H.Robinson

Asteraceae + + +

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 10Note : (+) Present ; (-) Absent; Land A1 = strong brown reclaimedland; Land A2 = black reclaimed; Land B = abandoned land.Family: Asteraceae = Compositae, Poaceae = GramineaeLamiaceae = Labiateae

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


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

The low species richness of understory vegetation inmined land was presumably caused by two factors. First,the land was only recently reclaimed or abandoned. InWestern Australia, Norman et al. (2006) found that thecomposition of vegetation in mined land had not matchedthat of the original vegetation, even after 14 years ofreclamation.Similar situation was found in Tomago, NewSouth Wales (Chaffey and Grant 2000). The second factormay be the low fertility of the mined land as shown by soiltest results (Table 2), indicating that all sites in general hadlow soil fertility.

Table 2. Soil pH, nitrogen, phosphorus and potassium content,and porosity

N-total P2O5

K-available

TotalporosityLand types pH-

H2O (%) (ppm) (me.100g-1) (%)Dark brown reclaimedland (A1)

4.3 0.16 3.21 0.1 48.605

Black reclaimed land(A2)

4.5 0.14 4.33 0.3 45.402

Abandoned land (B) 4.2 0.13 5.16 0.41 46.281

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

Species importanceSpecies importance was determined by the biomass.

The three most important or dominant species were Scleriasumatrensis, Eragrostis chariis, and Paspalum conjugatum,but they ranked differently in each land type (Table 3). Indark brown reclaimed land, the biomass of Scleriasumatrensis and Eragrostis chariis had much higherbiomass than the other species. Scleria sumatrensis is aperennial grass, has dense clumps, and may reach 2m inheight (Nasution 1986). A clump of this species may cover1 m2 of ground. Eragrostis chariis can grow in compactedstony soil, sandy soil, or clay. It has extensive and deeproot system so that it is hard to uproot. It may reach 1.25 inheight and it has many leaves near the ground (Sastrapradjaand Afriastini 1981). It was obvious that the two grasseswere capable of producing large biomass and couldtherefore dominate the areas.

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

Biomass (g.m-²)SpeciesA1 A2 B

Scleria sumatrensis Retz. 92.76 7.26 1.59Eragrostis chariis (Schult.) Hitchc. 19.07 2.52 1.79Paspalum conjugatum Berg. 1.39 10.75 1.35Chromolaena odorata (L.) R.M.King &H.Robinson

1.14 1.41 0.43

Eleusine indica (L.) Gaertn. 0.02 0.02 0.02Mikania micrantha H.B.K. 0.43 0.01 0.10Paspalum commersonii Lamk. 0.58 0.33 0.22Mimosa pudica L. 1.40 0.13 0Wedelia trilobata 0.11 0.27 0Polygala paniculata. L. 0.06 0.28 0Imperata cylindrica (Linn.) P. Beauv. 0.57 0.33 0Fimbristylis miliaceae (L.) Vahl 0 0.44 0Hyptis rhomboidea Mart. & Gal. 0 0.13 0Calopogonium mucunoides Desv. 0 5.46 0Pycreus sanguinolentus (Vahl) Nees 0 0.22 0.46Porophyllum ruderale (Jacq.) Cass. 0 0.09 0.03Pennisetum sp. 0 0 0.09Total 117.54 29.63 6.07Note: Land A1 = strong brown reclaimed land; Land A2 = blackreclaimed land; Land B = abandoned land.

In the black reclaimed soil, Paspalum conjugatum wasthe most dominant species, with much higher biomass thanthe other species. This species grows well in open space(Nasution 1986) as in this type of land. This species hasstrong root system and may reach 50 cm in height and has3-5 leaves in each node. It reproduces by seeds as well asby rhizome. Even in hard soil this species thrives(Sastrapradja and Afriastini 1980).

The biomass of reclaimed land was much higher thanthat of abandoned land (Figure 3). This might be due to theintroduction of mycorrhiza and nitrogen fixing bacteria andfertilization in the reclaimed land. Although both thereclaimed and abandoned mined land had low fertility, it ispossible that mycorrhiza and Rhizobium which might haveinfected the roots help the plants take nutrients from thesoil. It has been reported the addition of both Rhizobiumand mycorrhiza can increase the uptake of nitrogen,phosphorus and potassium by seedlings to be used forrehabilitation of mined land (Widyarti 2007). Reforestationof coal mined land in Ohio was successful due toinoculation of mycorrhiza (Cordell et al. 1999).

Composition similaritySØrensen’s Index (Table 4) showed that both reclaimed

mined had high similarity, which was 81%. This meansthat the species composition of both areas was relativelythe same. Both reclaimed land had moderately high (63%,and 69%) similarity index with abandoned mined land.When the composition of each mined land type wascompared with that of natural forests in Bukit Kaba(Loanita 1999) and in Lebong Selatan Sub District(Setiawan 1998), the indices showed zero values, meaningthat the species composition of understory vegetation inmined 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 35

for the success of restoration set by the Society ofEcological Restoration (Clewel and Aronson 2007). Thistotal difference indicated that mined land and natural foresthad different stage of succession. Mined land vegetationwas in the early stage of succession while natural forestwas in a climax stage, or in late stage of succession. Thespecies colonizing the mined land were pioneer species.Over time, these species will be gradually replaced by latesuccession species. In South Sumatra, even after 15 yearsof mined reclamation, the species composition of groundcover was still different from that of the natural forestnearby (Suhartoyo et al. 2012). In Australia, therehabilitated mined land, age 8-24 years, only had 12-37species in common with the adjacent natural shrub land(Herath et al. 2009).

Table 4. Species composition similarity of understory vegetationamong land types

Types of land compared ISs (%)

Strong brown reclaimed land and black reclaimedmined land

81.15

Strong brown reclaimed land and abandoned minedland

63.64

Black reclaimed land and abandoned mined land 69.23Reclaimed mined land and natural forest 0Abandoned mined land and natural forest 0

Note: ISs = SØrensen’s Index of Similarity,

Soil propertiesThe soil properties (Table 2) in reclaimed and

abandoned mined land showed low fertility (BalaiPenelitian Tanah 2005). All three sites were very acidic andhad low total nitrogen. Potassium levels were low in bothreclaimed land and medium in abandoned land. Thedifference, however, was very little. Phosphorus levelswere very low in reclaimed land and low in abandonedland. The porosity was medium for all sites. The sites hadlow fertility because the soil surface material was not topsoil, but mine spoil. The presence of vegetation for oneyear had not increased soil fertility. Other studies inSumatra also showed that newly reclaimed coal mined hadrelatively low soil fertility (Suhartoyo et al. 2012;Munawar 2003; Nurliana and Wiryono 2004). The soilcondition in this study site was not extremely harsh; somany species of pioneer plants invaded this site naturally.Some mine sites are so harsh that only few plants can growunless soil amelioration has been conducted (Bradshaw1997).

CONCLUSION

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

abandoned mined land. The species composition of twotypes of reclaimed mined land was similar to each otherand to that and abandoned mined land, but totally differentfrom that of natural forests.

ACKNOWLEDGEMENTS

We thank the management of Danau Mas HitamCompany who allowed us to do research in theirconcession area. We appreciate the help and suggestion ofGuswarni Anwar during our research. The valuablesuggestions from an anonymous reviewer are gratefullyacknowledged.

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BIODIVERSITAS ISSN: 1412-033XVolume 14, Number 1, April 2013 EISSN: 2085-4722Pages: 37-42 DOI: 10.13057/biodiv/d140106

Proposing local trees diversity for rehabilitation of degraded lowlandareas surrounding springs

SOEJONO1,♥, SUGENG BUDIHARTA1, ENDANG ARISOESILANINGSIH2

1Purwodadi Botanic Garden, Indonesian Institute of Sciences, Jl. Raya Surabaya-Malang, Km.65 Purwodadi, Pasuruan, East Java, Indonesia.Tel./fax: +62-341-426046, email: [email protected]

2Department 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 areassurrounding water spring. Biodiversitas 14: 37-42. This study was aimed to propose alternative trees diversity for rehabilitation ofdegraded 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 threesites were then compiled into an integrated list and used as reference for developing questionnaire. The questionnaire was thendistributed to respondents who were chosen randomly. We recorded their preferences of tree species in rehabilitation program based onsocio-economical and ecological aspects. Selected species were then proposed as alternative plants for rehabilitation of degraded springarea based on landscape topography and remaining vegetation coverage. The results showed that species diversity of Moraceae familywas 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 ValueIndex. 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 Ficusracemosa were the most preferred species by local community. Based on topography and vegetation coverage, spring surrounding areaswere classified into four: steep and open, flat and open, steep and dense, and flat and dense. Therefore among of 120 species found in allsampling sites, there were respectively 63.3%, 95%, 25% and 44.16% species to be proposed and planted for rehabilitation in the fourclassified areas.

Key words: Tree diversity, rehabilitation, degraded areas, spring

INTRODUCTION

The impacts of habitat degradation are not onlydecreasing plant and animal species diversity, but alsoaccelerating threatens ecological processes and naturalresources in short and long term, including declining waterquality and flow rate. It is known that water is an importantproduct of ecosystem services to humans, and its qualityand quantity depends on many factors; among them are thecarrying capacity of physical environment and quality ofvegetation coverage in the catchment area of spring.Therefore, conservation of plants diversity and ecosystems,both in situ, ex situ and rehabilitation of degraded areas isecological significant value.

Various efforts to rehabilitate degraded lands andforests in Indonesia held using diverse ways or scenariosby the parties, but in general they often plant and prioritizeexotic trees species, especially plant for timber productionpurposes, such as acacia (Acacia mangium), sengon(Albizia falcataria) and jabon (Anthocephalus cadamba)(Nawir et al. 2007). These plants will not grow longbecause it will be harvested to provide for wood needs, sothe impact of rehabilitation for the urgent purposes such assustainable environmental improvements and or ecological

service is poorly integrated. In addition, not allrehabilitated sites are ecologically, socially andeconomically suitable to be planted using limited speciesrichness as well as exotic ones, whereas, fault the plantschoice for rehabilitation, will lead to counter-productiveresults. Some researchers showed that in the areassuccessfully reforested with pine, residents complained thatthe well water was shrinking (Sumarwoto 2003). Yonky etal. (2003) mentioned that pine has a high value ofevaporation (1000-2500 mm year-1 ) depend on the locationand climate condition. It will cause water deficit in thewatershed, especially if it is planted in areas where rainfallis less than 2000 mm year-1. However, in areas with highrainfall (3308 mm year-1) as in Somagede, Sempor,Kebumen, where they studied, the pine forest is not causeof water shortages in the downstream. Controversy aboutthis is still often discussed, because pine is an exotic andplant providing not only for reforestation, but also expectedto support the success of business revenues, from wood andresin products (Yonky et al. 2003).

On the other hand, planting exotic plant, Acacia niloticain Baluran, is expanding rapidly. This plant is then known tobe invasive type (Hernowo 1999; Sabarno 2001; Iskandar2006; Zuraida 2011), so its control becomes a significant


problem. Djufri (2004) stated that the invasion of Acacianilotica has resulted in the reduction of savanna in BaluranNational Park reaching 50%. Pressure to the savannashowed a great impact on the balance and preservation ofwhole ecosystem in Baluran. Therefore this study wasaimed to propose plant diversity for rehabilitation degradedlowland area surrounding spring.


This study was conducted in three sites in the sub-districts Purwodadi, Pasuruan, East Java (Figure 1).Information of spring locations was obtained from the localpeople. Data were collected in three sites (1st Cowek, 2nd

Gajahrejo, 3rd Parerejo) for vegetation analysis usingMueller-Dombois and Ellenberg’s method as noted in(Soerianegara and Indrawan 1983) in order to determinedensity, frequency, dominancy, diversity index andImportant Value Index. Eleven plots of 1ha square shapewere observed for each site. The lists of plants in three siteswere then compiled into one integrated list and used asreference for developing questionnaire. The questionnaires

were then distributed to respondents chosen randomly inorder to record data on local community preferences inselecting tree species, viewed from social and economicaspects. Selecting tree species to be proposed forrehabilitation degraded lowland areas surrounding waterspring 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 ofcoverage). Based on topography and vegetation coverage,spring surrounding areas were classified into four: steepand open, flat and open, steep and dense, as well as flat anddense. Using these criteria, suitability of tree species wasdetermined using a rapid assessment and expert judgment,based on field observations and records of empiricalknowledge. This paper is an output of a thematicsubprograms research activity of Purwodadi BotanicalGardens in 2011/2012, entitled, Study of vegetation andrehabilitation of habitats surrounding spring in Pasuruandistrict, East Java, Indonesia.

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

Gajahrejo

Parerejo

Cowek

2

1

3

A

D

B C

SOEJONO et al. – Proposing plant diversity for rehabilitation 39

Table 1. Vegetation profile at three sampling sites around lowland spring in Districts Purwodadi, Pasuruan (Soejono and Budiharta2011, modified)

Variable 1st Cowek 2nd Gajahrejo 3rd Parerejo All sites

No. of families 30 28 23 33No. of genus 55 37 42 78No. of species 72 69 54 120Dominant family Moraceae Moraceae Moraceae MoraceaeDiversity index 5.08 5.06 4.5 -Co-dominant species and(% IVI)

Ficus racemosa (29.4),Ceiba pentandra (23.6),Artocarpus elasticus (18.1),Swietenia macrophylla (16.8),Ficus virens (16.8).

Bambusa blumeana (53.9),Dendrocalamus asper (41.2),Ceiba pentandra (26.6),Gigantochloa atter (15.4),Ficus benjamina (5.3).

Bambusa blumeana (91.4),Syzygium samarangense(25.7), Ceiba pentandra(21.9), Ficus virens (15.4),Dendrocalamus asper (12.9).

-

Density (ind. ha-1) 64 110 80 84.8


Ecological aspectsAt least there were 120 species of trees growing in

habitat around the lowland springs. It is known that thefamily Moraceae found as the highest species diversity thanothers, such as Ficus racemosa, also reached the highestimportance value index in the first site Cowek, whileBambusa blumeana showed the highest importance valueindex in the second and third sites (Table 1). Trees speciesreached high Importance Value Index (IVI) including Ficusracemosa, Artocarpus elasticus, Bambusa blumeana,Dendrocalamus asper, Gigantochloa atter, Ficusbenjamina, Ficus virens and Syzygium samarangense.

The average density of trees in the three sites were stillrelatively low, 64, 110 and 80 trees per ha. Lieberman andLieberman (1994) reported the results of their research thatthe total number of stems ≥ 10 cm dbh, enumerated in 12.4ha, a mean density is 446.0 individuals ha-1. Thisinformation is useful for determining tree density andspecies diversity existing in these sites, and then forestimating seedling density requirement for rehabilitationor restoration of degraded areas by considering theirecological and functional approach. According to Manan(1992), the best approach to restore diversity or forrehabilitation of degraded land was using the adjacentnatural community structure (primary forests) as avegetation model, especially in complexity, composition,vertical or horizontal stratification, richness, diversity andendemism rate. Consequently, the result of the successionacceleration by rehabilitation would be optimal as expectedand harmony under natural conditions. In general, the morediverse plant species and structure, the better its effect onsoil and water conservation.

Socio-economic aspectsSurvey was carried out to record data on community

preferences, involved 60 respondents from three samplingsites. In general, the results of survey showed that thespecies of Moraceae was a widely accepted by localcommunities for rehabilitation purpose of degraded areasaround the spring. The high level of preference of

respondents to the diverse species of Moraceae indicatedthat traditional knowledge on plant species commonlygrown around the spring is still preserved and it is inharmony with the ecological aspects. Besides Moraceae,respondents preferred local tree species producing variouseconomical benefits such as Durio zibethinus, Pangiumedule, Parkia timoriana, Aleurites moluccana, Artocarpusaltilis, Artocarpus elasticus as a producer of fruits or seeds,while Cananga odorata and Michelia champaca as aproducer of aromatic flowers. Examples of selected plantsfor rehabilitation of open area around the spring and socio-economic reason by local people are listed in Figure 2.

Figure 2. Some local tree species selected by local people forrehabilitation of open area around the spring and providing socio-economic benefits

From Figure 2, it showed that diversity of tree speciesof 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.

Plan

ts s

peci

es


Using a simple technology, seed germination and seedlinggrowth of Ficus benjamina, F. drupacea, F. racemosa, F.variegata and F. virens were successfully propagated byseeds (Soejono 2007). Main character of this genus wasshown in the fruit namely figs. The fruit is formed from thebase of the enlarged flowers and closed to form orbicular.The flowers are hidden inside the figs. The important thingto note that the most of Moraceae grown in lowlandtropics, even, some species of the genus of Ficus, estimatedthat its distribution centered located in the Indo-Malayregion, includes Indonesia. Some Ficus species are alsoknown to be classified as a keystone species, because fruitsare favored by wildlife as food. Therefore, these speciesshow a great potential, if planted as a material forenvironmental remediation (Sastrapradja and Afriastini1984; Berg and Corner 2005; Widyatmoko and Irawati2007).

In accordance to the restoration and control of waterresources, some species of Ficus show positivecharacteristics, such as, grow deep and broad rootingsystem, produce a dense branching in low position, developa broad canopy, that are potential to reduce speed ofrainfall drops. Thus destructive force to the surface layer oftop soil is lower, and the water infiltration to the ground isbetter. As a result, water is retained relatively longer in thesoil and released slowly, allowing the continuity of springand reduce erosion or landslides (Soejono 2011).Yulistyarini and Sofiah (2011) stated that quality of variousenvironmental services was depended on the density anddiversity of vegetation, soil type and its management. Theymentioned that, the high diversity of vegetation andthickness of litter will maintain hydrological function ofrecharge area and protect flow of water spring. Bruijnzeel1990 mentioned that environmental carrying capacity in thewater supply decreased, primarily due to changes invegetation coverage, related to change in the pattern ofevapotranspiration, infiltration rate, and the quality andquantity of surface flow. While Primack (1998) states thatsome important points in restoring degraded landcommunity, mostly relies on community efforts to re-establish native plants, because this plant communityusually produces most biomass and able to provide thestructure for other community members. Robinson andJohnson (2006) state that appropriate plant materials forrestoration by selecting species that are suitable for the site,grow from locally adapted sources, and have a solid geneticcomposition contribute to the success of project.

In line with this discussion, Bohnen and Galatowitsch(2005) stated that in most cases, high species diversity isrecommended for restoration to increase ecologicalfunction. The first preference is typically for seed andplants that come from similar site conditions, and as closeto the restoration site as possible. Edwards et al. (2010)introduced restoration model to support sustainablelivelihoods – building both environmental and socialresilience to climate change in the Shire Valley. Theycombined selected three multi-purpose species, Jatropha,neem and Moringa to spread risks and provide quickdiverse benefits.

Potential tree species diversity for rehabilitation basedon two criteria: topography and existing vegetation cover

Analysis of promising tree species based on topographyand existing vegetation cover, implemented by a rapidassessment (judgment), field observations and records ofempirical knowledge of the researcher team of PurwodadiBotanical Gardens, who often carry out field exploration invarious remote tropical primary rain forest and alsosupported by main literature (Backer and Bakhuizen 19651968; Heyne 1987; Soerianegara and Lemmens 1994;Soejono 2011; Narko et al. 2012). Landscape around thespring was divided into four simple groups based ontopography 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. Thereforeamong of 120 species found in all sampling sites, it wasnoted that: 63.3%, 95%, 25% and 44.16% respectivelywere proposed to be planted for rehabilitation in the fourclassified areas. Some examples of tree species proposedfor rehabilitation in the mentioned classified areas, arelisted in Table 2.

Table 2. Some examples of tree species showed a great potentialfor rehabilitation in the classified areas

Species

Stee

p an

d op

en

Flat

and

ope

n

Stee

p an

d de

nse

Flat

and

den

se

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 ● ●

SOEJONO et al. – Proposing plant diversity for rehabilitation 41

Tree species selection mentioned above, should alsoconsider ecological suitability in more detailed, includingsoil type, texture, structure and depth, climate, water useefficiency, as well as and autoecology of each species.Furthermore, the plant diversity for rehabilitation ofdegraded lowland areas surrounding spring was proposedby improving conventional replanting process using singlespecies, and considering different perspectives, such aspreserving plants diversity, prioritizing selection of localspecies, considering the ecological and socio-economicfunction, appreciating community preferences and adjusting tothe local areas conditions. Hopefully, this proposes cantechnically implementable, ecologically sustainable,economically profitable, socially acceptable and can bedeveloped in other places with similar conditions.

Cooperation and commitmentIn fact the success of rehabilitation in degraded areas is

not only determined by scientific considerations, but alsodetermined by the result of mutual cooperation andcommitment of all parties. To create synergies and optimizethe collective efforts in biodiversity conservation mana-gement, Donald (2013) reported that management actionneeded to be enriched by research and allowed researchersto learn from practitioners. In the implementation of itsactivities, it is important to coordinate with relevantagencies, landowners and apply certain approaches or anddissemination to the public. Moreover, planted seedlingsfor rehabilitation are also required regularly protection andmaintenance in early step until plants able to adapt to itsenvironment.

CONCLUSION

It can be concluded that there were 120 species of localtrees found in three sampling sites. Among them showedgreat potential as multipurpose plants and nominated bylocal people as material for rehabilitation of degradedlowland areas surrounding spring. Furthermore, thisalternative plant diversity for rehabilitation may improveconventional replanting process using single species, andconsider different perspectives, such as preserving plantsdiversity, prioritizing selection of local species, considerthe ecological and socio-economic function, appreciatecommunity preferences, adjust to the local areas conditionsand finally establish cooperation with various parties.Hopefully, this propose can be developed in other placeswith similar conditions for optimal and sustainableecological services of spring.

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Review: Current trends in coral transplantation – an approach topreserve 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

1National Institute of Oceanography and Fisheries (NIOF), Hydrobiology Department, P.O. Box 182, Suez, Egypt. Tel. +20 11 1072982, Fax. +20623360016, e-mail: [email protected].

2National 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 ofcoral mortality associated with the rise in stress factors and the lack of adequate recovery worldwide have urged recent calls for actionsby 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 mostfrequently 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. Newsurfaces can also be created through electrolysis. Molecular biological tools can be used to select sites for rehabilitation by asexualrecruits. Surface chemistry and possible inputs of toxic leachate from artificial substrates are considered as important factors affectingnatural recruitment. Transplants should be carefully maintained, revisited and reattached at least weekly in the first month and at leastfortnightly in the next three months. Studies on survivorship and the reproductive ability of transplanted coral fragments are importantfor coral reef restoration. A coral nursery may be considered as a pool for local species that supplies reef-managers with unlimited coralcolonies for sustainable management. Transplanting corals for making artificial reefs can be useful for increasing biodiversity, providingtourist diving, fishing and surfing; creating new artisanal and commercial fishing opportunities, colonizing structures by fishes andinvertebrates), 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 calciumcarbonate secreted by corals. They are also colonies of tinyliving animals found in marine waters that contain fewnutrients. Most coral reefs are built from stony corals,which in turn consist of polyps that cluster in groups. Coralreefs are fragile ecosystems, partly because they are verysensitive to water temperature. They face numerous threatsfrom climate change, oceanic acidification, blast fishing,cyanide fishing for aquarium fish, overuse of reefresources, and harmful land-use practices, including urbanand agricultural runoff and water pollution, which canharm reefs by encouraging excess algal growth. The coralreef ecosystem is a diverse collection of species thatinteract with each other and the physical environment. Thesun is the initial source of energy for this ecosystem.Through photosynthesis, phytoplankton, algae, and otherplants convert light energy into chemical energy. Asanimals eat plants or other animals, a portion of this energyis passed on. The Importance of corals and coral reefsinclude: (i) Corals remove and recycle carbon dioxide.

Excessive amounts of this gas contribute to globalwarming. (ii) Reefs shelter land from harsh ocean stormsand floods. (iii) Reefs provide resources for fisheries. Fooditems include fishes, crustaceans, and mollusks. (iv) Coralreefs attract millions of tourists every year. (v) The coralreef is an intricate ecosystem and contains a diversecollection of organisms. Without the reef, these organismswould die. (vi) Some evidence suggests that the coral reefcan potentially provide important medicines, includinganti-cancer drugs and a compound that blocks ultravioletrays. (vii) Coral skeletons are being used as bonesubstitutes in reconstructive bone surgery. The pores andchannels in certain corals resemble those found in humanbone. Bone tissue and blood vessels gradually spread intothe coral graft. Eventually, bone replaces most of the coralimplant. (viii) The coral reef provides a living laboratory.Both students and scientists can study the interrelationshipsof organisms and their environment.

Those very important coral reefs suffered sharp declinedue to several reasons which are both natural andanthropogenic. So, urgent strategies are needed to savecoral reefs, the most important of which is coral


transplantation. The purpose of the present work is toprovide a review for current trends in coral transplantationas a basis for preserving biodiversity.

NEED FOR CORAL CONSERVATION

The increasing rates of coral mortality associated withthe rise in stress factors and the lack of adequate recoveryworldwide have urged recent calls for actions by thescientific, conservation, and reef management communities(Rinkevich 2008; Teplitski and Ritchie 2009). In cases ofacute physical damage to reefs, such as in ship groundings,sophisticated engineering methods have been developed tomitigate damage and to maximize recovery and are used incombination with substrate stabilization and colonytransplantation (e.g. Jaap et al. 2006). Loss of live coralcover has been more related to abnormally high sea-surfacetemperatures and incidence of diseases, rather than directhuman activities (e.g. Miller et al. 2009). De Vantier et al.(2006) studied the indicators of management effectivenessin Bunaken National Park. On a global scale, the value oftotal economic goods and services provided by coral reefshave been estimated to be US$375 billion per year withmost of this coming from recreation, sea defense servicesand food production, that equates to an average value ofaround US$6,075 per hectare of coral reefs per year(Edwards and Gomez 2007). Degradation of reefs meansthe loss of these economic goods and services, and loss offood security to people living in coastal areas (Sutton andBushnell 2007). Reef restoration may face economic, legal,social and political constraints which are very much criticalto coral reef conservation policies like the ecologicalfactors (Job et al. 2003).

Recently, restoration strategies have focused on thebroader conservation effort, emphasizing the need tocombine local management actions, such as establishmentof no-harvest marine reserves and effective management ofthe coastal zone (both terrestrial and marine), with directactions, such as transplantation (Mumby and Steneck 2008,Bruckner et al. 2009). Transplantation of coral colonies orfragments, whether from aqua-, mariculture or harvestingfrom a healthy colony, has been the most frequentlyrecommended action for increasing coral abundance ondamaged or degraded reefs and for conserving listed or “at-risk” species (Teplitski and Ritchie 2009, Williams andMiller 2010). It has been suggested that newly developedmolecular tools be used to optimize selection of coralpropagules for cultivation and transplantation, to deepenour understanding of transplant survival (Baums 2008), andto identify and maximize the genetic diversity oftransplants (Ammar et al. 2000; Shearer et al. 2009), whichis considered essential. Debate continues over theeffectiveness of transplantation in conserving threatenedcoral species, increasing coral abundance, and acceleratingreef restoration or enhancement at ecologically relevanttemporal and spatial scales. This controversy is due in partto the small scale of transplant studies compared to thescale of reef damage (e.g. Edwards and Gomez 2007) andthe relatively short duration of most studies. Roeroe et al.

(2009) developed a coastal environmental assessmentsystem using coral recruitment. No coral conservationstrategy will be effective until underlying intrinsic and/orextrinsic factors driving high mortality rates are understoodand mitigated or eliminated (Garrison and Ward 2012).

REHABILITATION VS. RESTORATION

Rehabilitation can be defined as ‘‘the act of partially or,more rarely, fully replacing structural or functionalcharacteristics of an ecosystem that have been reduced orlost’’ (Precht 2006). It may also be the substitution ofalternative qualities or characteristics than those originallypresent provided that they have more social, economic orecological value than existed in the disturbed or degradedstate (Elliott et al. 2007) Thus, the rehabilitated state is notexpected to be the same as the original state or as healthybut merely an improvement on the degraded state(Bradshaw 2002). Ecosystem restoration has been definedby Baird (2005) as ‘activities designed to restore anecosystem to an improved condition. However, this doesnot imply the highest quality of the final ecosystem butmerely that it is better than the degraded situation. Becauseof this, a preferable definition of restoration is ‘the processof re-establishing, following degradation by humanactivities, 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 itspredisturbance condition and functioning.

TRANSPLANTATION OF STORM-GENERATEDCORAL FRAGMENTS

Transplantation of coral colonies or fragments, whetherfrom aqua-, mariculture or harvesting from a healthycolony, has been the most frequently recommended actionfor increasing coral abundance on damaged or degradedreefs and for conserving listed or “at-risk” species (Ammaret al. 2000; Rojas et al. 2008; Teplitski and Ritchie 2009;Shaish et al. 2010). Yet there is a deepening awareness thatno habitat, once damaged or degraded, can be restored toits original condition and that the basic factors causingdeclines must be addressed if restoration of reefs andconservation of threatened reef species are to succeed overtime (Bruno and Selig 2007). In response to dramatic lossesof reef-building corals and ongoing lack of recovery, asmall-scale coral transplant project was initiated in theCaribbean (U.S. Virgin Islands) in 1999 and was followedfor 12 years (Garrison and Ward 2012). The primaryobjectives were to (i) identify a source of coral colonies fortransplantation that would not result in damage to reefs, (ii)test the feasibility of transplanting storm-generated coralfragments, and (iii) develop a simple, inexpensive methodfor transplanting fragments that could be conducted by thelocal community. The ultimate goal was to enhanceabundance of threatened reef-building species on localreefs. Storm-produced coral fragments of two threatened

AMMAR et al. – Current trends in coral transplantation 45

reef-building species [Acropora palmata and A. cervicornis(Acroporidae)] and another fast-growing species [Poritesporites (Poritidae)] were collected from environmentshostile to coral fragment survival and transplanted todegraded reefs. Inert nylon cable ties were used to attachtransplanted coral fragments to dead coral substrate.Survival of 75 reference colonies and 60 transplants wasassessed over 12 years. Only 9% of colonies were aliveafter 12 years: no A. cervicornis; 3% of A. palmatatransplants and 18% of reference colonies; and 13% of P.porites transplants and 7% of reference colonies. Mortalityrates for all species were high and were similar fortransplant and reference colonies. Physical dislodgementresulted in the loss of 56% of colonies, whereas 35% diedin place. Only A. palmata showed a difference betweentransplant and reference colony survival and that was in thefirst year only. Location was a factor in survival only for A.palmata reference colonies and after year 10. Even thoughthe tested methods and concepts were proven effective inthe field over the 12-year study, they do not present asolution. No coral conservation strategy will be effectiveuntil underlying intrinsic and/or extrinsic factors driving highmortality rates are understood and mitigated or eliminated.

SAVING LARGE CORALS DURING THECONSTRUCTION OF A LIQUIFIED NATURAL GAS

PLANT

As parts of a mitigation measure associated with theconstruction of a Liquefied Natural Gas plant, four largecoral transplantations were carried out in Yemen betweenJanuary and October 2007 (Seguin et al. 2008). Around1,500 selected coral colonies were removed from areas tobe 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 kgup to 4 tonnes, were moved using new transplantationtechniques. Growth, in situ mortality and health of thetransplants were monitored over one year using photoquadrates, close-up pictures and linear growthmeasurements. Overall, survival of corals one year aftertransplantation was 91%. Most losses of transplants wereapparently due to sedimentation of fine particles in thetransplanted areas, fish predation, fisher activity and swelleffects. Evidence of coral growth after transplantation wasobserved, especially in Acropora and Porites species, andon some faviids. The transplantation results demonstratethe capacity of corals to adapt to a new environment, infavorable conditions. They show that carefully designedcoral reef rehabilitation strategies can be part of industrialdevelopment processes, whenever necessary.

TRANSPLANTATION OF JUVENILE CORALS

Clark and Edwards (1994) suggested thattransplantation of mature coral colonies may help restoredegraded reefs. However, such procedures cause damage to

other reef areas and are labor intensive. Knowledgeobtained on the reproductive patterns and settlingpreferences of the Red Sea corals (Benayahu et al. 1990)urged scientists to assess for the first time the potential useof their propagules for transplantation to an artificial reef.In addition, the unique autotomy process inDendronephthya hemprichi (Dahan and Benayahu 1997)facilitated the use of its fragments for this purpose. Thesurvivorship rates of transplanted species are related to thestructural features of the modular experimental artificialreef (Ammar and Mahmoud 2005).

MASSIVE VS BRANCHING CORALS

Branching morphologies are usually used inexperiments on coral regeneration for two main reasons:they have a life history with high asexual reproduction byfragmentation (Bruno 1998), and have rapid growth andregeneration (Karlson and Hurd 1993). They are also morefragile than other morphologies, often suffering the mostdamage from different stresses. The vertical arborescentstructure of branching Porites palmata was expected to besnagged, dislodged or damaged by seine net fishing to agreater extent than the spherical or horizontal encrustingstructure of P. lutea. Porites palmata is more susceptible tofish predation than the massive species. Massive corals arethus recommended for transplantation due to their lowdamage and mortality and may ultimately produce thehabitat required for fish and other coral morphologies.

SEXUAL REPRODUCTION IN TRANSPLANTEDCORAL FRAGMENTS

Studies on survivorship and the reproductive ability oftransplanted coral fragments are important for coral reefrestoration (Forsman et al. 2006). It is especially importantto determine the ideal collection time and minimumfragment size that are necessary for successful propagation(Kai and Sakai 2008). This is because the maximumsurvival rate with the possibility of spawning needs to beestablished in order to develop successful restorationtechniques. For example, aquariums try to establish coralbreeding facilities and nurseries using sexually reproducingcorals. Although several reports have stated that naturallyor artificially occurring fragments reduce fecundity or stopgonad development, those studies were performed onlyonce or just a few times after fragmentation (e.g. Zakai etal. 2000, Okubo et al. 2007). Survivorship and growth oftransplanted fragments have been surveyed and discussed(e.g. Yap 2004), but the spawning of fragments had neverpreviously been reported. Connell (1973) postulated thatthe occurrence of sexual reproduction in a colony isdetermined by the size of the colony or age of the polypscomprising the colony. Okubo et al. (2009) concluded thattransplantation of larger fragments during the cooler seasonresulted in an increased survival rate and spawning ratio inthe 1st year after transplantation in A. nasuta.


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

Figure 2. Big transplanted branches of Acropora (Photo’s copyright: Czaldy Garrote)

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TRANSPLANTATION OF CORALS USING SEXUALREPRODUCTION AND CERAMIC CORAL

SETTLEMENT DEVICE (CSD)

A new type of coral-restoration technology has beendeveloped since 1999 (Peterson et al. 2005, Okamoto et al.2005, 2008, 2010) to overcome bleaching and degradationcaused by global warming (Carpenter et al. 2008; Okamotoet al. 2007; Sato 2008). A case study was done by Okamoto etal. (2012) who conducted a survey of the coral communitystructure and recruitment of Acropora in six sites aroundManado, Indonesia, in 2007 and 2008. They found that thepopulation of Acropora corals as well as recruitment ofjuvenile coral was extremely low. To examine the future ofAcropora corals around Manado, they assessed thereproduction potential of Acropora at two sites of BunakenIsland. As a result, spawning was estimated to occurseveral times in 2007. Anyway, Isopora corals could not beseparated from Acropora (hereafter referred to asAcroporidae). The number of Acroporidae that settled onCoral Settlement Devices (CSDs) and Marine Block (MB)plates was very low. The spawning peaks of Acropora wereestimated to be between February and June, and aroundOctober. The spawning around October was lower than thatobserved between February and June. They attempted toapply a coral restoration method using sexual reproductiondeveloped and successfully applied in Japan’s largest coralreef, Sekisei Lagoon, to prevent the extinction of Acropora.For the experiments, they used CSDs to settle and raisecorals in situ for transplantation and MB plates as artificialsubstratum on sandy bottom areas. The ceramic coralsettlement device (CSD) contained within a polypropylenecase is fixed to the sea bottom 1 week before mass spawning.Settled corals were raised in situ for approximately one andhalf year (corals grew to approximately 1.5 cm in diameter).These corals were transplanted to coral reefs or onto marineblocks (MBs) on a sandy bottom. CSDs have been improvedby applying the results of in situ examination with regard tomaterials, shapes, and arrangement within a case. A smallCSD case makes the following features easy: underwaterhandling, deployment at the settlement site, and transportationto the nursery and restoration site. The CSD case is readilytransportable between the sea and the water tank onboard aship in a small plastic bucket filled with seawater.

INCREASING SUBSTRATE FOR SETTLEMENT

On a damaged reef, the availability of suitable substratefor larval settlement can rapidly decrease due to algal orsoft coral overgrowth, and sedimentation (Schlacher et al.2007). Minimizing land based sources of nutrientenrichment and maintaining algae-eating fish populationswill help reduce algae. Techniques for actively increasingsuitable substrate are briefly described below.

Introducing artificial surfaces for larval settlementArtificial reefs such as concrete blocks, wrecks or other

purpose-designed structures may have an additional benefit

for fisheries management but the cost may be prohibitivefor large areas.

Encouraging natural surfacesThis can be done by stabilizing or removing loose

substrate material (such as coral fragments) and removingalgae and other organisms that might inhibit larvalsettlement or damage young recruits. Certain substrates,e.g. Goniastrea skeletons, appear to induce settlement andlarval metamorphosis. This approach should only be takenif expert scientific advice is available.

Creating new surfaces through electrolysisA unique technology developed by a German architect

named Wolfe H. Hilbertz in 1977 involves precipitation ofionic calcium and magnesium in seawater to form acarbonate substrate under the presence of low direct currentunderwater (Hilbertz 1992). This substrate may serve as anatural platform for the transplanted corals and subsequentcolonization of marine larvae (Ammar 2001; Schillak et al.2001). The three hypotheses concerning growthenhancement mechanisms suggested by Hilbertz andGoreau (1996) are not fully explored experimentally. Thefirst hypothesis is that the electric field that enablesaccretion may cause the precipitated carbonates to attachdirectly to the skeletons of coral transplants. The second isthat the method induces CaCO3 enrichment of water in theimmediate vicinity of the coral, thereby enhancing naturalcalcification. The third one is that excess production andrelease of electrons due to the electrochemical processesoccurring within the vicinity of the coral might affect theelectron-transport chain for ATP production where theexcess energy can be used for growth enhancement. Thisrequires considerable financial and human investment, anda source of permanent electrical current while the structureis being built. The long-term impact of the electricalcurrent on marine life is not known.

Sabater and Yap (2002) investigated experimentally theeffect of electrochemical deposition of CaCO3 on linearand girth growth, survival and skeletal structure of Poritescylindrica Dana. Transplanted coral nubbins weresubjected to up to 18 V and 4.16 A of direct currentunderwater to induce the precipitation of dissolvedminerals. Naturally growing colonies showed a significantincrease in percentage of longitudinal growth over thetreated and untreated corals. Survival followed a similartrend as the growth rate. Lowest survival rates were foundin the untreated nubbins. Phenotypic alterations wereobserved in the treated nubbins where the basal corallitesdecreased in size with a concomitant increase in theirnumber per unit area. This was probably due to increasedmineral concentration (such as Ca2+ , Na-, Mg2+ , CO3

2-, Cl-,OH-, and HCO3-) at the basal region of the nubbins. Thesealterations were accompanied by a significant increase ingirth growth rates of the treated nubbins at their basalregions. The abundance of mineral ions at the basal regionthus appeared to be utilized by the numerous small polypsfor a lateral increase in size of the nubbins instead of alongitudinal increase.


CHEMICAL SIGNALS AND SURFACECHEMISTRY

The topics of surface chemistry (Spieler et al. 2001) andthe possible inputs of toxic leachate from artificialsubstrates were discussed and considered as importantfactors for enhancing natural recruitment (Ammar 2009).At least one artificial reef manufacturer (Reef Ball)recommended the addition of microsilica to concrete toprovide a neutral pH surface. In addition, the organic andmicrobial biofilm that is quickly formed on any clearsubstrate that is immersed in seawater may providenegative settling cues. It is also well documented that initialcolonizing microbial algal and invertebrate assemblagesmay affect settlement of coral larvae; moreover thechemical glycosaminoglycan isolated from a coralline alga(Hydrolithon boergesenii) that signals Agaricia agariciteshumilis larvae to settle, the synthesized material, called“coral flypa per”, proved effective for attracting larvae(Rinkevich 2005).

THREATS TO CORAL TRANSPLANTATION

Coral algal transition in coral transplantation experimentsYap et al. (2011) found that coral transplantation

experiments can provide a useful platform by which toexamine the overgrowth of coral by algae under differentenvironmental conditions. Macroalgae are well knowncompetitors 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 debatecontinues as to whether the algae themselves are capable ofoutcompeting, and then overgrowing, healthy coralcolonies. It is believed that algal spores or filamentsgenerally do not settle directly on live corals (McCook2001). However, when established algae come in directcontact with corals on the reef, this can cause shading,tissue abrasion, and/or overgrowth (Quan-Young andEspinoza-Avalos 2006). Abrasive contact or overgrowthcan eventually result in partial or total coral mortality. Livecorals are also capable of overgrowing algae (Diaz-Pulidoet al. 2009) and inhibiting algal growth (Nugues et al.2004). Once established, algal populations tend to persist,thus hindering reestablishment of coral populations viarecruitment (Kuffner et al. 2006) or the regrowth of adultcolonies.

Algal overgrowth is one major problem (Shaish et al.2010). It can be a significant factor that hampers thesuccess of coral restoration efforts because of reducedgrowth or mortality of the transplants. Under certainconditions, coral transplants appear unable to resist algalinvasion, and eventually die, apparently because ofsmothering (Dizon and Yap 2006). In some cases, algaewere observed to cause bleaching of the underlying coraltissue (Rojas et al. 2008). The bleached tissue subsequentlydeteriorated. Contact with algae can cause direct stress tocoral tissue, after which the algae proceed to overgrow thecoral (Quan-Young and Espinoza-Avalos 2006). Inexperiments where the performance of coral transplants in

the presence of algae was compared with that of corals incleared plots, transplants in the latter instances survivedbetter (Soong and Chen 2003).

Invertebrate corallivoresCros and McClanahan (2003) found the coral-eating

snail Drupella cornus on one block of transplants preyingon Porites palmata in the vicinity of a large patch of deadAcropora. There were three to four snails on eachbranching coral and they killed 60% of eachcolony/transplant, mostly at the base. This was similar toprevious observations of D. cornus preying on the genusAcropora and the family Pocilloporidae on damaged reefsin Kenya and Western Australia (Turner 1994). In the past,damage by Drupella outbreaks has been compared todamage by crown-of-thorns (COTs) outbreaks (Cumming1999). Reports of mass mortality due to this snail havebeen recorded in Western Australia and Japan (Turner1994). Outbreaks have been in part attributed to overfishing and the removal of key predators of the snail(McClanahan 1994).

ROLE OF AUTUTROPHS FOR TRANSPLANTEDCORALS

Primary producers, or autotrophs, make up the base ofall food chains, however, they are capable of synthesizingcomplex organic compounds such as glucose from acombination of simple inorganic molecules and lightenergy in a process known as photosynthesis (Baum et al.2003). The same author further indicated that somecommon autotrophs in a coral reef ecosystem arephytoplankton, coralline algae, filamentous turf algae, thesymbiotic zooxanthellae in corals, and many species ofseaweed. Phytoplanktons are one of the most importantprimary producers in the world and include a wide varietyof organisms. Those organisms include: 1-diatoms whichare the most productive type of phytoplankton 2-dinoflagellates and silicoflagellates which move by way offlagella 3-coccolithophores which have peels made ofcalcium carbonate 4-cyanobacteria, and other extremelysmall phytoplankton species referred to as nanoplankton(2.0-20 mm) and 5-picoplankton (0.2-2.0 mm). In brief, thephytoplanktons are important for providing transplantedcorals with complex organic compounds throughphotosynthesis.

REGENERATION AND GROWTH OF CORALFRAGMENTS IN A NURSERY

Soong and Chen (2003) indicated that one of theeffective and commonly used methods to restore coralcommunities is the transplantation of coral colonies orfragments. The same author, in this investigation, usedfragments of Acropora in a semiprotected nursery insouthern Taiwan between 1996 and 1998. The possibleeffects of different factors on the generation of newbranches and the initial skeletal extension rates of


transplants were tested. The variables under study were theorigin and length of the fragments, their new orientation,presence of tissue injury, and position in the fragment. Allthese factors were found to make a difference in either oneor both aspects of coral growth (i.e., branching frequencyand skeletal extension rate). These two factors clearlydetermine the success rate of a small fragment developinginto a large colony that has a much higher probability tosurvive and grow on its own. It was found the success ofcoral fragments in a semiprotected nursery depended onmany factors. With all factors taken into consideration, alarge amount of acroporid corals could be produced withina reasonable period. These materials can then be usedeither to restore natural populations directly or to satisfythe market demand for live corals, which would obviouslyreduce exploitation of natural populations.

Branching acroporids are known to translocate nutrientsdirectionally, which leads to faster extension rates of axialpolyps (Fang et al. 1989). Likewise, the ability of corals toregenerate was found to be dependent on the position of theinjuries in the colonies. In Acropora palmate theregenerative capability decreases away from the growingedge (Meesters and Bak 1995). In a multispeciescomparison, however, no position effect was found in theregenerative ability in six of seven species (Hall 1997). Theresults of orientation experiments on fragments withoutaxial polyps, however, indicate that the distal or proximalends in the original colony did not have any inherentadvantage in generating new axial polyps. Instead, the localenvironment determined the end at which new axial polypswere produced. It is possible that all the branches we usedin the experiment were distal branches of the colonies andthat the two ends of the 6-cm fragments posed littledifference in ontogenic gradients along the branches.Accordingly, whichever end pointed upward had a higherfrequency of generating new axial polyps. It may beconcluded that the resulting new branches are likely to bedistributed in the upper portions of fragments. Thischaracteristic is potentially adaptive in that branches inlower shaded regions of a colony tend to be overgrown andsmothered 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 forrehabilitation and for creating new fragments. The sourceof fragments must be chosen with care, to avoid damage toother reefs. Coral farms potentially have an additionalbenefit as an attraction for snorkelers. Further investigationis required to reduce costs and increase success rates. Theconcept of nursery installed on the sea floor has alreadybeen applied to corals (Rinkevich 2005). One of the majorex situ restoration approaches is the collection, settlement,and maintenance of planula larvae and spats under optimalconditions (Epstein et al. 2003). The in situ nurseryapproach sustains the mariculture of nubbins, coralfragments, and small colonies. A coral nursery may also beconsidered as a pool for local species that supplies reef-managers with unlimited coral colonies for sustainablemanagement (Epstein et al. 2003). Both ex situ and in situapproaches can also provide ample material for the coral

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

BIOGEOCHEMICAL PROCESSES AND NUTRIENTCYCLING WITHIN AN ARTIFICIAL REEF

Reef structures, by providing protection for marinespecies, 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 nutrientregeneration providing a nutritional source for other formswithin the ecosystem, or being exported by watermovements increasing the general productivity ofneighbouring areas, furthermore, planktivorous fish speciescan induce nutrient production in the water column,excreting substantial amounts of ammonium, urea anddepositing organic material, which is then incorporated intothe reef food web (Falcao et al. 2006).

SUCCESSFUL CORAL TRANSPLANTATION

For a successful coral transplantation, selection ofproper area to be used for transplantation is necessary(Okubo et al. 2005). It has been mentioned that thetransplantation might not be suitable in an area where thecoral recruitment has failed over the years. This is becausethe transplanted corals may not recruit. Also studies haveshown significant effects of environmental factors (eg.light, temperature, sedimentation and water movement) ongrowth and/or survival of coral transplants (Montebon andYap 1995; Palomar et al. 2009). Choice of a particularhabitat for coral transplantation is therefore a critical aspectof coral transplantation studies.

One more problem in coral transplantation is theselection of species to be transplanted. Studies have shownthat different coral species show different growth andsurvival after transplantation due to the differences in theirlife history strategies (Yap et al. 1992). Till now onlyselected species have been used in the transplantationstudies. But information on the suitability of a particularcoral species for transplantation and their responses torelocation needs to be established by more research.Edwards and Clark (1998) have argued that there has beentoo much focus on transplanting fast growing branchingcorals over slow growing massive corals. They furthermention that fast growing branching corals although recruitfast, are not able to survive the effect of transplantation andrelocation. Another factor to be considered in the coraltransplantation efforts is the size of coral colonies orfragments. In the previous studies, it has been shown thatthe size of the coral plays an important role in the survivalof transplanted fragments (Bowden-Kerby 1996, 2009).

However, the relationship between colony size andgrowth was shown to be significant for some species, butnot in others (Clark and Edwards 1995). Miyazaki et al.(2010) observed the survival and growth of transplantedfragments of the reef coral species Acropora hyacinthusand Acropora muricata over a period of 3 years from


Figure 3. Coral farming (Rinkevich 2005)

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

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November 1999 to November 2002 in a high-latitude coralcommunity in Shirigai National Marine Park, Otsuki,Kochi Prefecture, Japan. A total of 36 coral fragments (atotal area of 4.4 m2) (thirty one A. hyacinthus fragmentsand five A. muricata fragments) were transplanted into 3separate blocks at 3-4 m depth with each block consistingof approximately equal number of coral fragments in eachspecies. Out of 36 coral fragments transplanted, all A.muricata fragments died before the first survey (one yearafter the transplantation) and only 29 A. hyacinthusfragments survived the initial relocation. The resultsshowed an increase in the coral cover to 48% of the totalarea form the initial 8.9% in case of A. hyacinthus. Therewas a horizontal increase in the coral size resulting in theaccretion of the coral skeleton with the neighboring coralfragments. Transplanted fragments grew rapidly (6.9-15.8cm) in the warmer (17-25ºC) months compared to theslower growth (0.9-4.8 cm) in the colder (below 17ºC)months.

CONCLUSION

Coral transplantation should be carried out by peoplewith relevant experience. Prior to considering coraltransplantation, ensure that the transplant site is not subjectto ongoing impacting processes, such as strong waves,shallow water snorkel areas, crown-of-thorns (COTs)infestation, or shading by structures or vessels. Ensuredonor areas have a sufficient healthy and diverse coralcover. Total coral collection impacts must be within thenatural variability of the area and must not significantlyreduce the donor area coral cover or species composition.For the transplant site, identify and record the proposedspecies, numbers, sizes and placement of the individualcolonies to be transplanted. Document a methodology,addressing careful removal, fragmentation, handling andattachment of corals, and describing how impacts to livetissue will be minimized. Transplant all corals to the samedepth, aspect, habitat, water flow, proximity to adjacentcolonies and orientation as the site from which they wereremoved. Consider interactive impacts between adjacentcolonies. Tag, photograph and otherwise easily andaccurately identify each transplanted colony for theduration of the transplantation and at least 12 monthsfollowing completion of the project. Carefully maintain thetransplants. Revisit and reattach corals at least weekly inthe first month and at least fortnightly in the next threemonths. A coral nursery may be considered as a pool forlocal species that supplies reef-managers with unlimitedcoral colonies for sustainable management. Recoverabilitydepends on the stressor, the impacted species/communityand the temporal and spatial intensities of the stressor. thelarger the transplanted fragment, the greater the probabilityof survival (Garrison and Ward 2012). Transplanting coralsfor making artificial reefs can be useful in increasingbiodiversity; 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 issignificant and may reach several hundreds of milliondollars per year. Coral transplantation will not be effectivein conserving coral species or in assisting reef recoveryover time until the underlying factors causing degradationof reefs and mortality of corals are understood, addressed,and eliminated or mitigated.

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

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SPECIES DIVERSTYSpecies diversity of Selaginella in Mount Lawu, Java, IndonesiaAHMAD DWI SETYAWAN, SUTARNO, SUGIYARTO

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ECOSYSTEM DIVERSTYEndophytic fungi associated with Ziziphus species from mountainous area of Omanand new recordsSAIFELDIN A.F. EL-NAGERABI, ABDULQADIR E. ELSHAFIE, SULEIMAN S. ALKHANJARI

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Dynamics of fish diversity across an environmental gradient in the Seribu Islandsreefs off JakartaHAWIS H. MADDUPPA, BEGINER SUBHAN, DONDY ARAFAT, ADITYA BRAMANDITO

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Variability of soil physical indicators imposed by beech and hornbeam individualtrees in a local scaleYAHYA KOOCH, SEYED MOHSEN HOSSEINI, SEYED MOHAMMAD HOJJATI,ASGHAR FALLAH

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Species composition of understory vegetation in coal mined land in Central Bengkulu,IndonesiaWIRYONO, ARIF BUHA SIAHAAN

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Proposing local trees diversity for rehabilitation of degraded lowland areassurrounding springsSOEJONO, SUGENG BUDIHARTA, ENDANG ARISOESILANINGSIH

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REVIEWReview: Current trends in coral transplantation – an approach to preserve biodiversityMOHAMMED S.A. AMMAR, FAHMY EL-GAMMAL, MOHAMMED NASSAR, AISHA BELAL,WAHID FARAG, GAMAL EL-MESIRY, KHALED EL-HADDAD, ABDELNABY ORABI, ALIABDELREHEEM, AMGAD SHAABAN

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Biodiversitas vol. 14, no. 1, April 2013

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