1461Q 2003 Estuarine Research Federation

Estuaries Vol. 26, No. 6, p. 1461–1471 December 2003

A Comparison of Brachyuran Crab Community Structure at Four

Mangrove Locations under Different Management Systems along

the Melaka Straits-Andaman Sea Coast of Malaysia and Thailand

ELIZABETH C. ASHTON1,†,*, PETER J. HOGARTH2, and DONALD J. MACINTOSH1

1 Centre for Tropical Ecosystems Research, Department of Ecology and Genetics, Building 540, NyMunkegade, University of Aarhus, 8000 C, Denmark

2 Department of Biology, P. O. Box 373, University of York, York YO1 5DD, United Kingdom

ABSTRACT: Brachyuran crab community structure was compared between mangrove sites under different managementsystems from four locations along the Melaka Straits-Andaman Sea Coast. Klong Ngao, a mangrove estuary in RanongProvince of southern Thailand, lies within a Biosphere Reserve designated in 1997. Sites were positioned in plantationsat a former charcoal concession forest, a disused tin mine, and an abandoned shrimp pond along this estuary. TheMerbok estuary in Kedah, Malaysia, is partially managed: the mangroves are cut for charcoal and poles on a small scaleand the forests are left to regenerate naturally. The Matang Mangrove Forest Reserve in Perak, Malaysia, is heavilyexploited but well managed, for Rhizophora wood to produce charcoal, and has been for 100 years. Sites were positionedin plantations of different ages. Kuala Selangor Nature Park, Selangor, Malaysia, was established as a nature reserve in1987 and contains mature mangrove forest regenerating naturally from previous selective felling. At Klong Ngao andMatang, mature reserve forest sites were also studied for comparison with plantation sites. The sites included bothupstream and downstream locations and were of similar area, minimizing effects from possible species-area relationships.Sites were chosen with similar environmental conditions and with a dominance of Rhizophora spp. At each site perlocation, the brachyuran crabs were sampled quantitatively in 100 m2 quadrats by three independent 15-min timed crabcatches. The crab community recorded was analyzed by univariate and multivariate statistical techniques. Managementhistory plays an important role in moderating the crab community structure. The crab community also changes with theage of the mangrove forest stand. Sesarmid crabs consistently dominated in mature forests, whereas young plantationswere colonized mainly by ocypodid crabs. The findings show that heavily effected sites—e.g., disused tin mining areas,former concession forests, and abandoned shrimp ponds—can be rehabilitated by planting mangroves and that the crabcommunity is a useful ecological indicator of habitat status.

Introduction

Large areas of mangrove forest in Southeast Asiahave been destroyed or degraded over the past fewdecades. Thailand’s Andaman Sea coast lost142,200 ha between 1961–1989 (Aksornkoae et al.1993) and Peninsular Malaysia lost 18,700 ha be-tween 1980–1990 (Chan et al. 1993). The majorreasons for mangrove loss are population growth,conversion to aquaculture, agriculture, and coastalurban and industrial development (Clough 1993;Ong 1995; Field 1996; Macintosh 1996). The scaleof mangrove loss in Thailand up to 1986 was 64%(110,300 ha) due to the conversion to shrimpponds and 26% (45,200 ha) due to coastal devel-opments; other activities included salt ponds (6%)and tin mining (3%) (Aksornkoae et al. 1993).

* Corresponding author; tele: 145 8942 3341; fax: 145 89423350

† Current address: Institute of Aquaculture, University of Stir-ling, Stirling FK9 4LA, Scotland, UK. tele: 144 1786 467885;fax: 144 1786 472133; e-mail: e.c.ashton@stir.ac.uk

Large areas have also been selectively cut for char-coal, firewood, poles, and construction materials.

Poor shrimp farming practices, disease epidem-ics, and acid sulphate soils have led to many pondsbeing unproductive and left disused or abandoned(Macintosh 1996; Stevenson 1997). Salt ponds andtin mining areas have also been abandoned, cre-ating large areas of degraded land. Concern aboutthe loss of mangroves and increased awareness ofthe ecological, environmental, and socio-economicvalues of mangrove ecosystems—for example, inprotection against coastal erosion (Pearce 1996)and as feeding and nursery grounds for commer-cial fish and shellfish species (Chong et al. 1990)—has led to rehabilitation and restoration projects(Field 1996).

Field (1996; p. 17) defines restoration of an eco-system as ‘‘The act of bringing an ecosystem backinto, as nearly as possible, its original condition,renewing it or bringing it back into use.’’ Rehabil-itation on the other hand is a more general termto denote any activity, including restoration and

1462 E. C. Ashton et al.

habitat creation, which converts a degraded systemto a stable alternative (Stevenson et al. 1999). Man-grove forests can be managed for a variety of rea-sons; for example, commercial production of char-coal, coastal protection, or as bird sanctuaries, na-ture parks, or other reserves for the conservationof habitat and wildlife.

The success and failure of rehabilitation, resto-ration, and management projects are often not re-corded (Field 1996; Stevenson et al. 1999), butsuch information would help guide the planningand implementation of future conservation efforts.Success depends on the objectives of management,but it could be defined as reconstitution of the pre-vious state (this however is often unrecorded), orit could be defined as maintaining a sustainablefunctioning ecosystem. Assessing success is subjec-tive, but ecological indicators of habitat status thatcan easily be measured would be a useful tool tohelp managers record the effect of managementinterventions in mangrove forest ecosystems.

Brachyuran crabs are abundant and diverse con-stituents of mangrove forests ( Jones 1984). Theyplay an important role in the ecological function-ing of the mangrove ecosystem (Lee 1998),through litter turnover (Robertson 1986), seedpredation (Smith 1987), and bioturbation of thesoil (Smith et al. 1991), and also provide an im-portant food source for coastal fisheries (Macin-tosh 1984). For these reasons Smith et al. (1991)suggested grapsid crabs as possible keystone spe-cies. Mangrove crabs are also affected by physicaland biotic factors (e.g., Macintosh 1988; Hogarth1999; Lee 1999; Ashton et al. 2003). The objectivesof this study were to describe and compare the bio-diversity and community structure of brachyurancrabs at mangrove forest sites with different man-agement histories and regimes; and to determinewhether brachyuran crabs can be used as indica-tors of mangrove habitat status.

Materials and Methods

STUDY AREA

The four study locations in Southeast Asia wereKlong Ngao (9859N, 98839E) in southern Thailand,and Merbok (58309N,1008259E), Matang (48509N,1008379E), and Kuala Selangor (38209N, 1018159E)in Peninsular Malaysia. These locations lie alongthe Andaman Sea and Melaka (5Malacca) Straitscoastline of the Thai-Malay Peninsular.

The four locations are under different manage-ment systems. Klong Ngao forms part of a 30,000ha Biosphere Reserve established in 1997 for con-servation and sustainable use of its mangrove for-ests. The reserve is managed using a zoning systeminvolving three zones differing in the level of pro-

tection they provide. The core zones contain a to-tally protected forest (5,970 ha); buffer zones sur-round the core zones and include areas convertedpreviously for tin mining and more recently forshrimp farming (5,288 ha); while transition zonesinclude areas converted into roads, agricultureplantations, and residential areas (Thulstrup1998). Degraded areas are replanted using seed-lings reared in nurseries. The Merbok mangroveforests (5,400 ha) were designated as a forest re-serve in 1951 and are under the jurisdiction of theKedah State Forest Department (Ong et al. 1980;Wetlands International 1996). They are partiallymanaged; they are cut for charcoal and poles on alow scale and the forests are left to regenerate nat-urally. The Matang Mangrove Forest Reserve(40,200 ha) borders the Selinsing River in Perakand is heavily used but well managed for Rhizophoratimber to produce charcoal, and has been for 100yr. The forest is managed on a 30-yr rotation cyclewith thinnings at 15 and 20 yr. About 1,000 ha areclear felled annually in areas of a few ha. A 3-mbuffer zone is left along the riverbank to preventerosion (Gan 1995). Natural regeneration is assist-ed where necessary by planting seedlings reared innurseries. The Kuala Selangor Nature Park bor-dering the southeast shore of the Selangor Riverestuary was established as a nature reserve in 1987and the mangrove forest of about 300 ha has notbeen logged since then, except to provide accessvia walkways. It consists of primary forest near theforeshore and secondary forest inland with naturalregeneration (Chan et al. 1993).

In all four locations the climate is hot and hu-mid with high rainfall. The rainfall patterns aresimilar with a Southwest monsoon from April toOctober and a Northeast monsoon from Octoberto February. Ranong Province is the wettest placein Thailand with an annual rainfall of 4,200 mm atRanong City (Ranong Provincial MeteorologicalStation unpublished data), although this measure-ment is taken 10 km from the coast and at KlongNgao the rainfall is lower. The locations in Penin-sular Malaysia have lower annual rainfall (about2,000 mm) but Taiping 10 km inland from Matangis the wettest place in Peninsular Malaysia with anannual rainfall of 4,092 mm (Saad unpublisheddata). The highest astronomical tides are greatestfor Kuala Selangor and Klong Ngao at 5.4 and 4.4m, respectively, with those at Merbok (3.3 m) andMatang (2.7 m) lower but similar. Merbok wasstudied July–December 1995, Matang was studiedAugust–December 1997, Kuala Selangor was stud-ied June 20–July 12, 1999, and Klong Ngao July 15–August 3, 1999. The four mangrove locations coverconsiderably different total areas, with Kuala Selan-gor having the lowest area at 300 ha and Matang

Crabs as Indicators of Mangrove Management 1463

the highest at 40,200 ha. Sites of similar area wereselected in order to minimize possible species-arearelationships.

As far as possible, the sites selected also featuredsimilar environmental conditions and dominanceof Rhizophora trees, but with different managementhistories (Table 1). In Klong Ngao (KN) the siteswere a 10-yr-old Rhizophora mucronata Lamk. 1804plantation on a disused tin mine site (KNTin), 5-yr-old Rhizophora apiculata BL. 1827 (KNCRa) andR. mucronata (KNCRm) plantations on an area pre-viously designated as a concession area for timberextraction for charcoal production and a sevenyear old mixed Rhizophora spp. plantation in anabandoned shrimp pond (KNSh). More details ofthe Klong Ngao sites are provided in Macintosh etal. (2002). In Merbok (MB) Rhizophora zonationwas observed and sites were used from a tributaryupstream called Sungai Pasir (MBSP) and thendownstream the Merbok estuary at Upper Merbok(MBUM), Middle Merbok (MBMM) and LowerMerbok (MBLM) (Ashton 2002). The sites had afew large mature trees (.40-yr old). In Matang(MT) a young (7–10 yr old) and mature plantation(30-yr old) were sampled upstream (U) and down-stream (L) of the Selinsing river. In Kuala Selangor(KS) a Rhizophora zone was sampled upstream(KSR) and downstream (KSS). The seaward sitewas adjacent to an old collapsed walkway. In bothKlong Ngao and Matang a mixed mature reserveforest site was also chosen as a reference site forthe plantations and to assess the extent of regionaldifferences in the fauna (KNRes and MTRes, re-spectively).

DATA COLLECTION

A 100 m2 vegetation quadrat was sampled ateach site. Within each quadrat the number of man-grove tree and sapling species and the number ofindiv within each species was determined (Tomlin-son 1986). The circumference at breast height ofeach individual was recorded and from this thecross-sectional area, or basal area (BA), was calcu-lated (English et al. 1994).

Replicate measurements (n 5 3 to 10) of envi-ronmental variables were made in each vegetationquadrat. The number of senescent and decayingleaves was recorded from ten 1-m2 quadrats. Soilpore water salinity was recorded using a refractom-eter, soil temperature recorded using a thermom-eter, and tidal inundation regime recorded usingthe method of English et al. (1994).

Crabs were sampled quantitatively by conductingthree independent time-based collections in every100 m2 vegetation quadrat. The crabs were sam-pled at low (spring and neap) tide, with the as-sumption that brachyuran crab faunas do not

change significantly over this time scale (Ashton etal. 2003). The method devised by Ashton (1999)was found to provide a good representative sampleof the crustacean population present at the site.Crab catch per unit effort was one 15 min catchper person. The area covered in each 15 mintimed period was approximately one-third of the100 m2 quadrat. As many crabs and types of specieswere caught as possible; this was best done by handusing a trowel and a plastic beaker. To reduce biastowards common or slow-moving crabs, more timeand effort was allocated to catching the less com-mon or elusive species. The crabs were put intolabelled resealable plastic bags and carefully trans-ported back to the laboratory. The crabs were putin the freezer to sedate them before they were de-scribed and then preserved in 4% formalin for lat-er species identification.

DATA ANALYSIS

The vegetation univariate data calculated foreach site using the species abundance data weretotal number of species present, Shannon-Wienerdiversity index, and the Simpson’s dominance in-dex. The environmental data were tested for sig-nificant differences between the sites using a one-way analysis of variance (ANOVA) followed by aTukey-Kramer multiple comparison test, where ap-propriate. If the data could not be transformed tonormality a non-parametric Kruskal-Wallis test wasused. The environmental variables were correlatedusing the Spearman rank correlation.

Crabs were described using the univariate mea-sures of abundance, number of species, Margalef’sspecies richness, Shannon-Wiener diversity indexcalculated using loge, and Pielou’s evenness.Where necessary, univariate measures were trans-formed using log or log 1 1 to normality and dif-ferences between sites was tested using a one-wayANOVA, followed by a Tukey-Kramer post hoc test.A lower triangular similarity matrix was construct-ed using the Bray-Curtis similarity coefficient onnon-standardised, square-root transformed crusta-cean data. Formal significance tests for differencesbetween sites were performed using the one-wayANOSIM permutation test on the crab similaritymatrix (Clarke and Green 1988; Clarke 1993). Thecrab species contributing to dissimilarities betweenthe sites were investigated using the similaritiesprocedure (SIMPER) (Clarke 1993). PRIMER(Plymouth Routines In Multivariate Ecological Re-search) software package was used for these statis-tical analyses (Clarke and Warwick 1994).

Relationships between the crab communitystructure, the forest structure and managementand the environmental variables were assessed withCanonical Correspondence Analysis (CCA) (Ter

1464 E. C. Ashton et al.

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Crabs as Indicators of Mangrove Management 1465

Braak 1986), using the software package Multi-Var-iate Statistic Package (MVSP), ver. 3.1 (Kovach1998). The CCA ordination technique uses trendsin crab species similarity to produce a matrix,which is shown for each site as points on a biplot.The sites are also related to ordinations of collect-ed environmental, vegetation, and managementparameters that are plotted as additional axes inthe direction of the trend defined by the parame-ter concerned.

Results

VEGETATION

Table 1 gives a summary of the forest manage-ment and vegetation characteristics at each of thestudy sites. The exact ages of the plantations inKlong Ngao and Matang are known and at bothlocalities the mangrove trees in each site are simi-lar in age. The mangroves in the other sites studiedincluded trees of different age classes and their agecould only be estimated from past records. TheMatang reserve site is known to be the oldest pro-tected site but some of the trees at Merbok andKuala Selangor may be of a similar age. The basalarea of the trees followed the same pattern as theage of the stands with the Matang Reserve Foresthaving the greatest values followed by the Merboksites, the Klong Ngao Reserve site and the 30-yr-old plantations in Matang. The Kuala Selangorsites had lower basal areas than expected for theirage, probably reflecting the effects of selective tree-felling that seems to be on-going even though it isnow illegal.

In the study sites the number of mangrove treespecies was low and dominance of Rhizophora spp.high. The Klong Ngao Reserve forest and the Kua-la Selangor River transect had the highest tree di-versity and lowest dominance. The lowest tree di-versity and highest dominance was found atKNCRa because the site was 100% R. apiculata. TheKuala Selangor Sea transect had the lowest Rhizo-phora dominance (28%).

The stem density was greater in the young plan-tations, as expected, since the trees were youngerand therefore more dense but smaller in averagesize. Mangrove seedlings are planted in Matang at1.2 m intervals, but there is also natural regener-ation (Gan 1995). At the Klong Ngao shrimp pondseedlings were planted by students sometimes asclose at 0.1 m 3 0.1 m (Macintosh et al. 2002).The Klong Ngao charcoal concession and tin min-ing sites were planted at 0.5 m 3 0.5 m intervalsbut problems with weeds in the former site (Mac-intosh et al. 2002) and in the latter deep tidal in-undation (Macintosh personal observation) andpoor soil properties (Komiyama et al. 1996), re-

sulted in a lower survival rate and density. The Kua-la Selangor Sea transect also has a high stem den-sity because of the large number of saplings thathave established near the disused walkway. Theother, older sites have low densities, because of nat-ural thinning, or thinning in the course of forestmanagement.

ENVIRONMENT

Mean values for the environmental variablesmeasured are shown in Table 1. All the environ-mental variables were significantly different be-tween the sites (p , 0.001) and many of them werecorrelated. Soil temperature ranged from 258C atthe Lower Merbok site to 288C at the Klong Ngaotin mining site. Soil temperature was negativelycorrelated with the number of senescent and de-caying leaves (rs 5 20.37, p , 0.001, and rs 520.24, p , 0.01, respectively). The Klong Ngao tinmining site had the least leaf litter both of senes-cent and decaying leaves at 1 m22. The highestnumber of senescent leaves were recorded fromthe Lower Merbok and Matang Reserve sites andthe highest number of decaying leaves were re-corded from the Matang downstream 10-yr-old siteand the Matang Reserve site. The numbers of se-nescent and decaying leaves were highly correlated(rs 5 0.57, p , 0.001). The low salinities recordedat the KNRes site and the Matang upstream plan-tations were due to the presence of a stream whichreceived a large influx of freshwater during thesampling period. Salinity was positively correlatedwith tidal inundation (rs 5 0.41, p , 0.001). Thenumber of days the sites were tidally covered eachyear was significantly lower at the Matang sites. Themost exposed site was MTL10, which was sub-merged only during extreme high tides. In con-trast, the low-lying former tin mining plantationwas covered by every high tide. Tidal inundationwas also positively correlated with soil temperature(rs 5 0.37, p , 0.001) and negatively correlatedwith the number of senescent (rs 5 2040, p ,0.001) and decaying leaves (rs 5 20.55, p ,0.001).

CRABS

Thirty-one brachyuran crab species were record-ed from the study sites. This included 18 grapsidspecies, 11 ocypodid species, and 2 pilumnid spe-cies. Nine species were recorded from only onesite, 7 of which were only from Klong Ngao inThailand. No species were recorded from all thesites, but Clistocoeloma merguiense De Man 1888 andSesarma (Perisesarma) onychophorum (De Man 1895)were widely distributed, being recorded from all 4locations and from 14 of the 16 sites.

The sites differed significantly in total crab abun-

1466 E. C. Ashton et al.

TABLE 2. Mean univariate measures 6 SD of crabs caught per person in 15 min for each of the study sites and results from oneway ANOVA between sites. Site abbreviations as in Table 1.

Abundance Species Richness Diversity Evenness

Klong NgaoResTinCRaCRmSh

15 6 4.041 6 1246 6 2052 6 2722 6 13

5.3 6 1.53.7 6 1.26.3 6 2.97.0 6 1.04.3 6 0.58

1.6 6 0.410.71 6 0.251.5 6 0.901.6 6 0.391.2 6 0.30

1.4 6 0.330.38 6 0.01.1 6 0.821.5 6 0.22

0.99 6 0.16

0.83 6 0.000.30 6 0.000.55 6 0.340.76 6 0.110.69 6 0.16

MerbokSPUMMMLM

5.0 6 1.78.0 6 6.110 6 3.210 6 3.2

2.3 6 1.55.0 6 3.65.7 6 1.53.0 6 1.7

0.74 6 0.851.8 6 1.12.0 6 0.48

0.86 6 0.76

0.66 6 0.671.3 6 0.781.5 6 0.41

0.75 6 0.65

0.94 6 0.000.91 6 0.000.89 6 0.100.81 6 0.00

MatangResU7U30L10L30

5.3 6 3.25.7 6 2.57.7 6 0.588.0 6 1.721 6 3.2

2.3 6 1.23.0 6 0.02.0 6 1.02.7 6 0.584.7 6 1.2

0.91 6 0.911.3 6 0.46

0.48 6 0.480.80 6 0.261.2 6 0.43

0.65 6 0.581.0 6 0.0

0.49 6 0.450.67 6 0.221.1 6 0.47

0.89 6 0.160.94 6 0.000.82 6 0.000.68 6 0.000.68 6 0.19

Kuala SelangorRS

7.3 6 2.57.7 6 1.2

3.3 6 0.584.3 6 0.58

1.2 6 0.141.7 6 0.36

1.2 6 0.142.3 6 0.23

0.96 6 0.000.87 6 0.00

F valuep value

9.38,0.001

2.74,0.01

1.660.11

1.850.07

4.79,0.001

dance, species number, and evenness (Table 2).The Klong Ngao plantations KNTin, KNCRa, andKNCRm had the highest crab abundances. TheKNCRm plantation supported a significantly high-er number of crab species than MTU30, andKNTin had significantly lower evenness than all theother sites. One-way ANOSIM results between thestudy sites for the brachyuran community similaritymatrix also show that the Klong Ngao tin miningsite and shrimp pond site plantations containedbrachyuran crab communities significantly differ-ent in structure to those in all the other sites. Thetwo charcoal plantation sites at Klong Ngao werenot significantly different from each other, butwere from all the other sites.

Similarities percentages analyses of square-roottransformed brachyuran crab abundance data re-vealed that the sites at Matang had the highest sim-ilarity (50%) and the sites at Klong Ngao the lowest(27%). The plantations had the highest crab com-munity structure similarity—for example MTL30(68%), KNTin (67%), and KNSh (64%)—and thenaturally regenerated sites the lowest—for exam-ple, MBSP (16%) and KNRes (26%). The discrim-inating species that contributed to 60% dissimilar-ity between all pairwise plot combinations areshown in Table 3; there are 20 species in total. Thediscriminating species for each site have been not-ed. The crab community in the former tin miningsite in Klong Ngao was more than 90% dissimilarto all the other sites. It is discriminated by the high

abundance of Metaplax elegans DeMan 1988 andthe presence of Tylodiplax tetralyphora De Man1895, found only at this site. The Klong Ngao char-coal sites are discriminated by the high abundanceof Uca triangularis (A. Milne Edwards 1873) andUca rosea (Tweedie 1937), whereas the other siteswere predominantly grapsid crabs. Klong Ngao re-serve site was discriminated by high abundances ofC. merguiense and Sesarma lenzii (De Man 1894) andlow abundances of a number of sesarmid species.

The brachyuran crabs were divided into grapsidsand ocypodids. Figure 1 shows the grapsid and ocy-podid crab abundances between the study sites.There was a significantly greater (F 5 10.6, p ,0.001) number of grapsid crabs at the Klong Ngaotin mining plantation than at the other sites. Thiswas because of the dominance of M. elegans. Ocy-podid crab abundance was also significantly differ-ent between the study sites, with sites KNCRa andKNCRm having higher densities than the othersites (F 5 7.7, p , 0.001). There were no signifi-cant differences in the number of grapsid speciesbetween the study sites, but the number of ocy-podid species was significantly different (F 5 6.1,p , 0.001), with the highest recorded from KNCRaand KNCRm (Fig. 1).

The abundance of grapsid and ocypodid crabsare plotted against tidal level (computed as thenumber of days per year each site is tidally inun-dated). Figure 2 shows that both the abundance ofgrapsid and ocypodid crabs was not related to tidal

Crabs as Indicators of Mangrove Management 1467

Fig. 1. Mean number of grapsid and ocypodid crabs caughtper person in 15 min collecting periods in each study site 6SE.KN 5 Klong Ngao; MB 5 Merbok; MT 5 Matang; KS 5 KualaSelangor; Res 5 reserve forest; Tin 5 tin mining area; C 5charcoal concession area; Sh 5 shrimp pond area; SP 5 SungaiPasir; UM 5 Upper Merbok; MM 5 Middle Merbok; LM 5Lower Merbok; U 5 upstream; L 5 downstream; 7, 10, 30 5age of plantation; R 5 river transect; S 5 sea transect; Ra 5Rhizophora apiculata; Rm 5 R. mucronata. a) abundance and b)species.

Fig. 2. Mean number of grapsid and ocypodid crabs caughtper person in 15 min for each site against the tidal inundation(number of days covered by tide each year). a) abundance andb) species.

Fig. 3. Biplot illustrating the relative position of each siteand the brachyuran crab community structure with the environ-mental and forest management characteristics. Site abbrevia-tions are: A 5 KNRes, B 5 KNTin, C 5 KNCRa, D 5 KNCRm,E 5 KNSh, F 5 MBSP, G 5 MBUM, H 5 MBMM, I 5 MBLM,J 5 MTRes, K 5 MTU7, L 5 MTU30, M 5 MTL10, N 5 MTL30,O 5 KSR, P 5 KSS.

level. The same pattern was obtained for the num-ber of species present.

Figure 3 shows the canonical correspondenceanalysis biplot of the brachyuran crab speciesabundance for each site as the points in relationto the environmental and forest management char-acteristics plotted as arrows. Tidal cover varies in-versely with the number of senescent leaves alongaxis 1, while on axis 2 soil temperature, tree diver-sity, tree age, and tree basal area vary in the op-posite direction to tree dominance. The KlongNgao tin mining site clearly separates out from theother sites in the direction of high soil tempera-tures. The Klong Ngao reserve site and charcoalconcession sites show a relationship with tree dom-inance and tidal cover. The other sites are clus-

1468 E. C. Ashton et al.

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basal area, and tree diversity.

DiscussionThis study demonstrates that the brachyuran

crab fauna reflects habitat status when naturalmangrove forests and plantation forests are com-pared, although it is difficult to clearly separatenatural (environmental) differences between siteswith management-induced ones. Within the con-straints and limitations of the sampling, two aspectsof management appear to affect the brachyurancrab community structure most strongly: the pre-vious history of the site and the age of the foreststand.

Biogeographical and regional influences on thefaunal assemblages studied are minimised becausethe locations are on similar latitudes (38 to 98) andlongitudes (988 to 1018). The mature reserve sitesin Klong Ngao, Thailand, and Matang, Malaysia,did not have similar crab species compositions (Ta-ble 3). The sampling method employed may nothave been able to record all crab species presentbecause the Matang reserve site had a high stand-ing crop of leaf litter. Assessment of the densityand diversity of burrowing crabs in mangrove hab-itats presents formidable methodological prob-lems. Total excavation and extraction by sieving isgenerally impractical, for logistical reasons as wellas the destructive nature of the method. Visual ob-servation and burrow counts provide at best crudeestimates of population density, even where a sin-gle species is concerned (Macia et al. 2001; Skovand Hartnoll 2001). Neither visual observationsnor burrow counts can readily be applied to multi-species assessment. The time-based crab samplingmethod used in this study is subject to both qual-itative and quantitative bias, and does not aim toprovide exhaustive census information on the spe-cies present. It does provide a rapid and practicalassessment, which if applied at different sites, en-ables between-site comparison of multi-speciescrab fauna to be made.

The low frequency of tidal inundation at Matangmay be a reason for the absence of some crab spe-cies from this location. Mangrove crabs are wellknown to show a zonation of species with shorelevel ( Jones 1984; Macintosh 1988): in the presentstudy we found the abundance or number of crabspecies was not influenced by tidal level per se (Fig.2). The high frequency of tidal inundation andhigher soil temperatures are contributing to thedifferent crab community structure present at thetin mining site in Klong Ngao, but these are alsothe result of past management practices (Macin-tosh et al. 2002).

The number of environmental factors recorded

Crabs as Indicators of Mangrove Management 1469

was limited and did not include others of possibleimportance to crabs, such as soil particle size, hy-drogen sulphide concentrations, and redox poten-tial. Environmental measurements should be treat-ed with caution; they only give a general indicationof conditions because they vary with the time ofday, and in relation to tidal inundation, seasons,and weather (Ashton et al. 2003).

Tree age, tree basal area, and tree diversity werecorrelated with the brachyuran crab communitystructure. Brachyuran crab community structurechanges with the age of the stand. High ocypodidcrab abundance and species number dominate dis-turbed and younger plantations, whereas largeabundances and species numbers of grapsidcrabs—in particular sesarmid crabs—dominatemature forests once the canopy closes. Similar pat-terns have been found elsewhere in Malaysia andThailand (Berry 1972; Macintosh 1984; Aksorn-koae et al. 1993; Sasekumar and Chong 1998). Ak-sornkoae et al. (1993) concluded that tree fellingand regeneration were responsible for much of theobserved disturbance and variation in the faunalcomposition. It is probable that the textural qual-ities of the soil change rapidly once mangrove veg-etation becomes established, and that burrowingcrustaceans are an important element in the pro-cess that leads to the soil becoming suitable forother species to colonize (Berry 1972).

Relatively few mangrove species have been usedin restoration projects; species of the genus Rhizo-phora are the most commonly used (Field 1996).Ong (1995) commented on an apparent declinein production at Matang and speculated that theremay be an ecological price to pay for the presentform of management because of the dominance ofRhizophora spp. Increased habitat heterogeneityand mangrove species diversity may support amore diverse crab fauna. The heavily managed Ma-tang mangroves and the previously heavily man-aged Klong Ngao mangroves have brachyuran crabcommunity structures significantly different fromthose of the less heavily exploited Merbok andKuala Selangor mangroves. Matang had the lowestcrab species number. The management has main-tained a functioning ecosystem, perhaps at a re-duced level of diversity. The long-term manage-ment and consequent homogeneity of the habitatmay contribute to this low crab diversity.

Tan and Ng (1994) suggest the maintenance ofhigh crab species diversity is integral to the healthof the mangroves. Natural and human-induced dis-turbances pose serious threats to the functioningof mangrove ecosystems (Osborn and Polsenberg1996). The reaction of natural ecosystems to dis-turbances is often non-linear, discontinuous, deter-mined by chance events, and therefore unpredict-

able (Holling et al. 1995). It is unknown at whatpoint human alteration has direct and irreversibleeffects and which components are critical to sus-tainability (Wells 1998).

Disused tin mining sites, former concession for-ests, and abandoned shrimp ponds can become re-colonized by a diverse and abundant crab fauna(Macintosh et al. 2002). Macintosh (1984) record-ed an annual total production for high densities ofU. rosea in a cleared Malaysian forest to be similarto low densities of S. onychophorum in a mixed for-est. The degraded areas can increase in productiv-ity and ecological functioning with reforestationbut care must be taken because density does notnecessary reflect biomass and secondary produc-tion (Macintosh 1984). Recolonization is possiblebecause crustaceans have larval stages with goodrecruitment potential into the intertidal zone(Macintosh et al. 1991). In addition, adults canmove into new habitat from nearby mangrove sites.Areas of mangrove near rehabilitation sites may actas sources of recruitment; this may be importantfor successful mangrove restoration. It is not clearwhat factors control the crab community structurethat develops.

In 1985 before the tin mining site was replantedthere were virtually no crabs (Macintosh personalobservation). After 10 yr a crab fauna is present,dominated by one species M. elegans. M. elegansprefers soft silty sediment and lower shores (e.g.,Tesch 1918; Jones 1986). The ecosystem has notbeen restored to a mature condition, but replant-ing has brought the ecosystem back into use. Fur-ther time may change the crab community struc-ture, or the anthropogenic effects may have madeirreversible changes preventing reversion of theecosystem to its original state. Aksornkoae et al.(1993) gives examples of the environmental im-pacts of mining on the plant and benthic com-munity structures in Thailand. Mangrove refores-tation was slow and seedling mortality high com-pared to mangrove plantations in natural dis-turbed mangrove forests. The faunal successionwas complex because species show different re-sponses to environmental stresses, and because op-portunistic species recolonize more quickly thanothers. The benthic community appeared to havereached equilibrium after 17 yr but with persistentdifferences from the original community structure(Aksornkoae et al. 1993).

The brachyuran crab community composition ata site may give an indication of the habitat status.High dominance of a species may indicate a stress-ful environment, whereas a high diversity of grap-sid crabs, especially sesarmids, may indicate a ma-ture forest (Macintosh et al. 2002). Ghost crabshave been used as a tool for rapid assessment of

1470 E. C. Ashton et al.

human impacts on exposed sandy beaches (Barros2001). Given the environmental complexity of con-ditions it is doubtful if one or two species could besufficiently sensitive to all major impacts affectingcomplex ecosystems, such as mangroves, to serveas indicator species. Monitoring changes in com-munity structure provides an alternative and moreeffective approach to assessing ecosystem health(Cairns et al. 1993). Brachyuran crab communitiesare ubiquitous throughout the region and are animportant component in mangrove food webs;they are also good indicators of local conditionsbecause of their sedentary nature and reasonablylong life cycles. Changes in brachyuran crab com-munity structure could be a useful tool for man-agers to detect mangrove habitat status.

Past and present management practices play animportant role in moderating crab abundance, di-versity, and composition. Further monitoring willincrease the knowledge and understanding on thestructure, dynamics, and resilience of mangroveecosystems. More rigorous approaches to the as-sessment of past and current restoration effortsmust be developed (Stevenson et al. 1999) and fur-ther research is required to understand the eco-logical effects of disturbance to mangrove forestsand whether changes in crab community structurewith management are consistent in other locations.

ACKNOWLEDGMENTS

This work was funded by a U.K. Darwin Initiative grant anda British Natural Environment Research Council grant for theMerbok and Matang studies and by DANCED (Danish Co-op-eration in Environment and Development) under the Danish-SE Asian Collaboration in Tropical Coastal Ecosystems Researchand Training (Denmark, Thailand, and Malaysia) project (ref-erence number 1230324) for the Klong Ngao and Kuala Selan-gor studies. We are very grateful to the collaborators—Dr. Ru-pert Ormond, York University; Mr. Sopon Havanon, Head ofthe Mangrove Forest Research Centre at Ranong; and ProfessorOng Jin Eong and Dr. Gong Wooi Khong at Universiti SainsMalaysia—for their assistance with research at Merbok; Dr.Chong Ving Ching and his team at Universiti Malaya for theirassistance at Matang; and Rasainthiran Menayah, Kuala Selan-gor Nature Park Manager, for his assistance at Kuala Selangor.We would also like to thank everyone else involved with thisresearch, including students from York University, and Thai andMalaysian project staff and fishermen. Comments from the re-viewers were invaluable and help from Garnet Hooper (StirlingUniversity, U.K.) and Thomas Nielsen (CenTER, DK) with theCCA plot.

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Received for consideration, December 3, 2001Revised, June 20, 2002

Accepted for publication, April 9, 2003