Biodiversity and abundance of terrestrial isopods along a gradient of disturbance in Sabah, East Malaysia

European Journal of Soil Biology 42 (2006) S197–S207 http://france.elsevier.com/direct/ejsobi

Original article

Biodiversity and abundance of terrestrial isopods along a gradient of disturbance in Sabah, East Malaysia M. Hassalla,*, D.T. Jonesb, S. Taitic, Z. Latipid, S.L. Suttond, M. Mohammedd a

Centre for Ecology Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7JT, UK Soil Biodiversity Research Group, Entomology Department, British Natural History Museum, Cromwell Road, London SW7 5BD, UK c Istituto per lo Studio degli Ecosistemi, Consiglio Nazionale delle Ricerche, Via Madonna del Piano, 50019 Sesto Fiorentino, Florence, Italy d Tropical Biology and Conservation Institute, University of Malaysia Sabah, Beg Berkunci 2073, 88999 Kota Kinabalu, Sabah, Malaysia b

Available online 20 July 2006

Abstract Connell’s intermediate disturbance hypothesis predicts that the highest diversity is maintained at intermediate levels of disturbance. We have examined this hypothesis by observing differences in biodiversity of terrestrial isopods along a gradient of disturbance from two undisturbed primary tropical rainforest sites, to a logged site, a mixed native fruit orchard and a commercial oil palm plantation, in Sabah, East Malaysia. We describe a standardised protocol for the rapid assessment of isopod biodiversity on tropical forest floor sites and for measuring environmental variables to which we have related differences in species richness and relative abundance of the isopods. The results do not support Connell’s hypothesis because there were no significant differences in diversity, species richness or equitability between disturbed sites and the nearest primary forests. The relative abundance of individual species was highest in the most disturbed environment. We suggest that this may be because particular species are well adapted to exploiting resources under the more ‘r’ selection conditions created by disturbance. Possible reasons for why the observations do not conform with predictions from the intermediate disturbance hypothesis are discussed. We conclude that Huston’s dynamic equilibrium model is more appropriate than the intermediate disturbance hypothesis in predicting the effects of disturbance of tropical rainforests on these arthropod macro-decomposers. © 2006 Published by Elsevier Masson SAS. Keywords: Diversity; Species richness; Equitability; Tropical rain forest; Logging; Deforestation; Dynamic equilibrium hypothesis

1. Introduction Primary tropical forests contain the highest biodiversity of any ecosystem on earth, but they are currently being lost at an unprecedented rate of 200,000 km2 each year [44]. In many systems disturbance creates spaces more suitable for earlier successional species. If disturbance is uniform and severe it can result in a relatively simple community of pioneer species with * Corresponding

author. Fax: +44 1603 59 1327. E-mail address: [email protected] (M. Hassall).

1164-5563/$ - see front matter © 2006 Published by Elsevier Masson SAS. doi:10.1016/j.ejsobi.2006.07.002

good colonising ability. When the disturbance is variable in time and/or space it may result in a mosaic of habitat patches at different successional stages. At a landscape scale such patchy communities are often more diverse than either uniformly heavily disturbed ones or completely undisturbed communities dominated by fewer highly competitive species. This principle is encapsulated in the ‘intermediate disturbance hypothesis’ [9] initially formulated in relation to tropical rainforests and coral reefs [8] but subsequently supported by studies of many other ecosystems [4,17,19,57,72] and recently thoroughly evaluated

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in relation to tropical forests by Sheil and Burslem [56]. While evidence of support for this hypothesis comes from the study of biodiversity of above ground communities in tropical forests [5,8,23] much less is understood about how disturbance affects the soil biota. Arthropods comprise the majority of the known biodiversity of tropical forest and 75% of these arthropods are found in the soil [10,59]. Termites are one of the major ecosystem engineers in many tropical soils and are very sensitive to changes in microclimatic conditions. Forest canopies buffer the forest interior from extreme variations in microclimate [20,62]. Temperature, relative humidity, wind speed and solar radiation at ground level are all highly sensitive to changes in canopy depth and structure [6]. Therefore, the buffering capacity is reduced if disturbance causes the canopy to become more open. Quantitative measures of vegetation structure and habitat modification suggest that as the degree of canopy loss increases, so an increasing number of forest-dependent termite species are exposed to microclimatic conditions outside their tolerance range, causing a decline in the survival and reproductive success of their colonies leading to eventual local extinction [34]. Studies on ants provide no clear or consistent evidence to support the idea that sites exposed to intermediate levels of disturbance have a significantly higher species richness than undisturbed sites of the same habitat type [2,12,21,42,53,68,69,71]. However, composition of ant communities does change following disturbance, with some old-growth forest specialist species being replaced in the disturbed forest and converted forest sites by open-habitat specialist and generalist species. When adopting a functional group approach, cryptic species and specialist predators are especially sensitive to even low levels of disturbance, while other groups show a positive or a more complex or variable response to disturbance [29]. The changes in the abundance and biomass of soil animals do not necessarily mirror changes in species richness. Disturbance within the forest in Cameroon had little effect on abundance and biomass of termites [15] although these were strongly reduced on cleared plots as also found in Indonesia [34]. Although earthworm species richness may be lower in primary forests than in grasslands which may replace them following prolonged disturbance, their biomass can be significantly higher in primary forests compared with disturbed polyculture plantations [28]. In this paper we examine both the diversity and abundance of terrestrial isopods as model arthropod

decomposers in order to test the intermediate disturbance hypothesis in primary rainforests and anthropogenically disturbed woodlands in East Malaysia, South East Asia. We present a protocol for rapid assessment of biodiversity in terrestrial isopod communities and results for five contrasting habitats representing a gradient of disturbance from primary forest through to oil palm plantations. 2. Materials and methods 2.1. Study sites Sampling was undertaken in October 2000 on five sites in three areas of Sabah, Malaysia: Danum Valley, Sepilok Forest Reserve, and Segaliud-Lokan oil palm plantation. The maximum distance between the three areas was about 80 km. ● Danum primary forest: the Danum Valley Conservation Area, in south-eastern Sabah (4°58′N, 117°48′E; altitude c. 100 m a.s.l.), consists of 43,800 ha of Class 1 primary lowland mixed dipterocarp forest, and has a mean annual rainfall of about 2800 mm [70]. The sampling site was 1500 m inside the forest along the West Trail. ● Danum logged forest: Coupe 1991 logging concession is an area of Class 2 lowland mixed dipterocarp forest selectively logged in 1991 (i.e. 9 years before sampling). This site has extensive logging trails alongside patches of forest showing different degrees of disturbance. The logging trails have highly compacted soil. The site was roughly 15 km from the primary forest site in the Danum Valley Conservation Area. In Sabah, selective logging involves removing all mature trees (> 60 cm DBH) of commercial species (about 8–15 trees per ha). Typically, logs are removed to the road or storage areas by bulldozer, with as much as 30–40% of the area disturbed by the bulldozers (and thus left as skid trails), and 40–70% of remaining unlogged trees incurring damage [46]. This form of selective logging represents an extremely high level of forest disturbance resulting, at the landscape level, in a mosaic of secondary forest at different stages of regeneration. ● Sepilok primary forest site: the Kabili-Sepilok Forest Reserve (15°45′N, 117°45′E; altitude c. 100 m a.s.l.) is situated 5 km from the east coast of Sabah adjoining the Sandikan Bay and consists of 4294 ha of primary lowland mixed dipterocarp forest, with a

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mean annual rainfall of about 3100 mm [18]. The mean daily temperature is 30 °C, and relative humidity up to 90%. There are more than 450 tree species in the reserve including 40% of the known dipterocarps recorded in Sabah [7]. The sampling site was approximately 1000 m from the nearest forest edge and 1 km from the orang-utan rehabilitation centre along the waterfall trail. ● The Sepilok orchard was a managed fruit tree garden, approximately 2 km from Sepliok Forest Reserve. The orchard consisted mainly of mature trees of rambutan (Sapindaceae Nephelium lappaceum L. 1767); mangosteen (Guttiferae Garcinia mangostana L. 1753), Durian, (Bombacaeae Durio sp.); Jackfruit, Moraceae Artocarpus heterophyllus Lam 1789 and Terap (Moraceae Artocarpus elasticus Reiw. 1825). ● The oil palm (Elaeis guineensis) plantation was situated next to the Segaliud-Lokan Forest Plantation research site (5°37′N, 117°35′E; altitude c. 100 m a.s.l.). The oil palm plantation covers 36 ha and is surrounded by Acacia mangium plantation and selectively logged forest. The oil palm plantation was established in 1990 and the palms were planted at 9 m spacing in a triangular pattern with 143 palms ha−1. Activities such as harvesting, pruning, manuring and insecticide spraying are common in the plan-

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tation. Prior to the establishment of the plantations, the site was lowland mixed dipterocarp forest. Further details of the soil and vegetation of the five sites are given in Table 1. 2.2. Rapid biodiversity assessment protocol At each of the five sampling sites, one grid of 100 m × 10 m was established in a representative area of the habitat. Grids were subdivided into 20 blocks along the length of the grid, each 10 m wide × 5 m long. Blocks were then divided into rectangles each 2 m wide × 5 m long. Rectangular plots were sampled on a stratified random basis, with one plot of 2 m × 5 m selected randomly in each 5 m block of the grid. 2.2.1. Sampling for relative abundance A 40 cm × 40 cm box quadrat was placed quickly on the randomly chosen coordinates then very rapidly processed to minimise disturbance and escape of jumping and rapidly running species. First the litter, then the fermentation layer and then the top Ah layer of soil were transferred rapidly into labelled polythene bags to be hand-sorted in a large (approximately 30 cm × 60 cm × 10 cm high) white tray in the laboratory within 24 h of sampling. All isopods from each layer were collected using battery powered aspirators

Table 1 Habitat characteristics of sampling sites. Means (± 1 S.E.) not sharing the same letter differ with P < 0.05

Vegetation Number of trees >10 cm diam 10 m−2 Dominant families or genera in:

Soil/litter profile pH at surface of Ah horizon Depth (cm) of Slope Aspect (bearing)

Danum Primary

Danum Logged

Sepilok Primary

Sepilok Orchard

Oil Palm

F

DoF

P

2.1ad ± 0.33

2.68a ± 0.28

4.2b ± 0.34

1.55cd ± 0.18

1.15c ± 0.08

21.048

4, 94

< 0.0001

Canopy and understory layers

Dipterocarpaceae, Dryobalanops, Shorea, Bamboo

Macaranga

Shorea,

E. guineensis (Leguminacae)

Ground layer

Marantaceae, Pandanaceae, Zingiberaceae, Bamboo

Zingiberacae, Annonaceae

Costus and Marantaceae

N. lappaceum, Axonopu compressus, Melastoma malabatrichun Melastoma Malabatrichun, Graminae

Pteridophytes, Leguminasae, Graminae

4.6ac ± 0.09

5.3b ± 0.23

4.2a ± 0.04

4.9bc ± 0.20

4.6ac ± 0.22

4.791

4,83

0.002

5.91 ± 0.35 1.73 ± 0.15 15.5a ± 1.2 176a ± 14

6.27 ± 0.50 1.83 ± 0.14 9.5b ± 1.0 229a ± 32

7.22 ± 0.46 1.93 ± 0.19 14.6a ± 1.4 188a ± 31

2.92 ± 0.50 1.47 ± 0.14 4.5c ± 1.4 198a ± 27

1.43 ± 0.32 1.59 ± 0.06 7.5bc ± 0.8 77b ± 5

32.28 1.577 15.5 5.472

4,88 4,94 4,93 4,79

< 0.0001 0.187 < 0.0001 0.001

L and F layer Ah layer

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and stored in labelled tubes of 70% alcohol with 5% glycerol.

3. Results 3.1. Habitat characteristics

2.2.2. Sampling for total biodiversity A further 10 min was spent by two experienced isopod collectors sampling by hand the most likely habitats for isopods, such as in damp hollows and adjacent to buttress roots, in the randomly chosen 2 × 5 m plot. Using a trowel, specimens and as much of the surrounding soil or litter as was necessary to secure the specimen, were placed in a fourth labelled polythene bag. 2.2.3. Recording habitat characteristics Ten centimetres from the four corners of the 40 cm × 40 cm quadrat the depth of the littler, F and Ah layer were recorded and the gradient and aspect of the slope measured. The dominant species and % cover of each layer of vegetation (ground (0–1 m), lower canopy and understory (1–15 m), middle canopy (15–40 m) and emergent (> 40 m) layers) immediately above the 2 × 5m plot were estimated by an experienced observer. pH was measured for soil from the surface 5 cm of the profile, using a digital probe pH meter in the laboratory. 2.3. Identification and characterisation of species Species identifications were based on morphological characters. All the collected specimens were separated into morphospecies after examination of the whole animals under a stereoscopic microscope and of micropreparations of their appendages and male characters (pereopods and pleopods). For some species of Armadillidae, observations were made under a scanning electronic microscope. Identifications of already known taxa and categorisation of new taxa were made using the relevant literature for the Oniscidea from the Oriental Region [1,16,27,33,35–37,39,43,47,52,54,55,63– 66]. A re-examination of most of the taxa described by Herold [27] and deposited in the Zoological Museum, Berlin, was necessary. 2.4. Analyses Diversity was measured using the Shannon–Weiner index H′ and equitability using Shannon J′ given by J0 ¼ H0 =log2 S Where S is the total number of species in the sample. Multiple regression, partial correlations and analyses of variance using GLM were conducted in SPSS version 11.

The density of trees over 10 cm DBH was highest in the Sepilok primary forest followed by the logged forest and the primary forest at Danum Valley (Table 1). In the primary forest at Danum the dominant trees were in several genera of the Dipterocarpaceae, with bamboo dominating in a gap caused by the fall of a large tree. Members of the Shorea genus were dominant in Sepilok primary forest. In all three of the forest sites the ground layer vegetation was dominated by young tree seedlings but in the orchard and oil palm sites more by grasses and herbaceous vegetation. pH varied significantly between the sites. It was highest in the logged forest at Danum and lowest in the primary forest at Sepilok (Table 1). The litter and fermentation layers were deepest in the primary forest at Sepilok and deeper at all three of the forest sites than at either the orchard or oil palm sites. The ground sloped significantly more steeply in both primary forest sites than in the disturbed sites. All the three forest and the orchard sites were approximately south facing while the oil palm site had a more easterly aspect (Table 1). 3.2. Diversity and equitability The mean diversity indices for plots in each of the sampling sites is given in Fig. 1a which shows that isopod diversity was on average significantly higher in the two Danum Valley sites than in the three other sites. There was no significant difference in diversity between the disturbed sites and the corresponding primary forests. Even in the most disturbed site, the oil palm plantation, the diversity was not significantly reduced compared with the Sepilok primary forest site, although the equitability index was lowest for this site (Fig. 1b). 3.3. Species richness A total of 26 species were collected (Table 2) of which 17 were new to science, including one new genus. Most species, 12, were found in the Danum primary forest and 11 in the Danum logged forest but of these only five were also found in the primary forest. In the Sepilok primary forest only four species were found, two of which were also found in the Danum Valley primary forest. Seven species were found in

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Fig. 1. a) Diversity (Shannon–Weiner index) of isopods at five locations along a gradient of disturbance in woody habitats in Sabah, East Malaysia; F4,95 = 13.49, P < 0.0001; b) the Shannon index of equitability (J′) F4,95 = 9.51, P < 0.0001) c) species richness (number of species collected from 10 m2 plots as described in the assessment protocol) F4,95 = 8.92, P < 0.0001. Means not sharing the same letter differ with P < 0.05.

the mixed native fruit orchard and four in the oil palm plantation. When expressed as mean number of species per plot (Fig. 1c) there were slightly, but not significantly, more species per plot in the Danum logged forest than in the Danum Primary forest. However, for both Danum sites there were significantly more species per plot than at the other three sites, among which there were no significant differences. Stepwise multiple regression and partial correlation analyses showed pH to be the only environmental vari-

able to which number of species per plot was significant related (b = 0.278, df, 65, P = 0.023). Of the different morphological types found, the largest species were all ‘runners’ [50] in the genus Burmoniscus. Most runners (seven) were found at the Danum logged site with five in the Danum Primary Forest where there were most ‘rollers’(six) (Table 2) and also a jumping species capable of jumping to a height of more than 20 cm which was one of the most abundant species there.

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Table 2 Species collected from each sampling site along the gradient of disturbance Numbers

Armadillidae Armadillidae Armadillidae Armadillidae Armadillidae Armadillidae Armadillidae Armadillidae Armadillidae Eubelidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Philosciidae Styloniscidae Trachelipodidae 5 Families

Genus

Reductoniscus Tuberillo Hybodillo Nesodillo Sumatrillo “Spherillo” Genus 1 Genus 2 Genus 2 Saidjahus Burmoniscus Burmoniscus Burmoniscus Burmoniscus Burmoniscus Burmoniscus Burmoniscus Burmoniscus Burmoniscus Burmoniscus (?) Pseudotyphloscia Papuaphiloscia Papuaphiloscia New genus Clavigeroniscus Nagurus 15 genera

Species

tuberculatus n. sp. sp. cfr. silvestris sp. hypotoreus sp. sp. 1 sp. 2 n. sp. angusticauda javanensis curvifrons orientalis n. sp. 1 n. sp. 2 n. sp. 3 n. sp. 4 n. sp. 5 n. sp. 7 n. sp. 1 n. sp. cfr. n. sp. n. sp. riquieri (?) sundaicus 26 species

Jumper

Clinger

Runner

Roller

X X X X X X X X X X X X X X X X X X X X X X X X X

X

1

X 1

15

10

Maximum length (mm) 5 4 5 7 8 3 7 2.5 4 12.5 11 7 7 7 6 4 10 6.5 16 8 4 5 5 4.5 3 5

Danum Primary

Danum Logged

Sampling sites Sepilok Sepilok Primary Orchard X

Oil Palm Estate

X X X X X

X X

X X X X

X X X

X X X X

X X X

X X X

X

X X X

X

X X

X

12

X X X 11

4

X 7

X 4

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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26

Family

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Fig. 2. Relative abundance of isopods along a gradient of disturbance in woody habitats in Sabah, East Malaysia. F4,95 = 5.379, P < 0.001. Means not sharing the same letter differ with P < 0.05.

3.4. Abundance The relative abundance of isopods on the five sites showed a reverse trend compared with the species richness, in that least individuals were collected from the primary forest sites and significantly more from the most disturbed oil palm plantation site (Fig. 2). Relative abundance in the logged forest in Danum Valley was similar to that in the adjacent primary forest and that in the mixed native fruit orchard was intermediate between that in the adjacent primary forest and that in the oil palm plantation. Multiple regression analysis showed that of all the environmental variables, the total number of isopods collected per plot was only significantly related to depth of litter layers (b = –0.366, df 61, P < 0.001), confirming that the abundance of isopods was lowest where the litter layer was thickest in the three forest sites. 4. Discussion Disturbance can be an important mechanism for maintaining biodiversity [31,32,58] with recent controversy concerning tropical rainforests clarified by Sheil and Burslem [56]. Large clearings and edges of forests often have more species associated with them than closed canopy forest [40]. However if such edge effects exist for terrestrial isopods they did not extend into the larger scale disturbances caused by logging and forest replacement on these sites. This suggests that for terrestrial isopods in these south east Asian forests and derived sites, the intermediate disturbance hypothesis was not supported. The mean number of species found per plot (Fig. 1b) did not differ significantly between any of the disturbed sites and the nearest pri-

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mary forest, and the highest total number of species was found in one of the primary forest sites (Table 2). Primary forest sites had a higher diversity of larger trees characteristic of climax vegetation with deeper litter layers and less ground layer vegetation (Table 1) than disturbed sites where there was a more open canopy and more fluctuating micro-climatic conditions at the soil surface. For other taxa disturbance can lead to an increase in diversity due to disruption of the complex competitive interactions that can develop in undisturbed systems and creation of opportunities for invasion of the community by generalist species replacing specialist endemic species characteristic of intact systems [23,41]. It is important to consider the scale both of the disturbance and of the observations of its effects when interpreting such changes. Hamer and Hill [22] found that increasing scale of observations resulted in a more rapid increase in total butterfly species observed in undisturbed forests than in logged ones. Hence while disturbance might appear to increase diversity at a small scale of observation, at a larger scale diversity actually decreased as a result of the same level of disturbance, perhaps because invading generalists had a wider distribution within the disturbed habitat than more specialised endemic species restricted to smaller patches in the undisturbed sites. In deciding upon the appropriate scale of study it is important to consider the mobility of the study species [38]. Many butterflies are capable of moving for hundreds of metres in a day so a scale of study in kilometres may be appropriate. Frugivorous birds may travel several kilometres in a day so a scale that is appropriate to the patchiness of the resources they are using would be necessary. Isopods have more restricted mobility. Unlike termites and ants they do not have a winged dispersal phase. Their daily trivial movement is thus measured in metres [29,45] so a study area 100 m long is more appropriate although extremely small in relation to the scale of disturbance in these forest sites. Of the species at the logged secondary forest site, 55% were not present in the corresponding primary forest site and of those at the orchard and oil palm sites 86% and 75%, respectively, were not found on the nearest primary forest site studied (Table 2). This suggests, considering the low colonising potential of this group, that species which may have existed below detectable levels in the primary forest, perhaps in gaps and were better adapted to the harsher conditions, increased as the closed canopy specialists declined when the canopy opened.

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The response of ants to disturbance in tropical forests is similar to that of isopods as sites with intermediate levels of disturbance do not have a significantly higher species richness than undisturbed sites of the same habitat type [2,12,21,42,53,68,69,71]. However, community composition does change upon disturbance, with some old-growth forest specialist species being replaced in the disturbed forest and converted forest sites by open-habitat specialist and generalist species. Other soil animals in tropical rainforests have also been found not to follow the predictions of the intermediate disturbance hypothesis, for example assemblages responding to disturbance in tropical forests (reviewed by Jones et al. [34]). In West Africa [14,73] and Southeast Asia [34], termite species richness was highest in the original primary habitat and correlated negatively with increasing habitat disturbance. A closed or very dense forest canopy is one of the key factors favouring high species richness of termite assemblages [13]. In the rain forest zones of Southeast Asia and West Africa, very few species occur that are preadapted to the harsher, drier conditions found in highly disturbed and forest-derived habitats, and so there are very few species which could replace forest-adapted species [34]. Similarly in Danum Valley the diversity of earthworms decreased in disturbed areas (V. Standon, pers. comm.). The significantly higher abundance of isopods observed at the most disturbed site could potentially be explained if the species there had different life history characteristics to those in the primary forest. Terrestrial isopods can be categorised into two groups, steneodynamic and eurydynamic, accordingly to their suites of life history characteristics and their intrinsic rates of natural increase [61]. Steneodynamic species are mostly small soil dwellers with a relatively narrow range of rf values whereas eurydynamic species are larger, more surface active and with a much wider range of rf values so able to increase in density much more rapidly in response to an increase in favourability of their habitat. In this study the blind colourless Pseudotypholoscia, and Papuaphiloscia which live deep in the humus layer [67] share some fundamental similarities morphologically and in habitat to typically steneodynamic temperate species such as Trichoniscus pygmaus and Platyarthrus hoffmanseggi. Similarly Saidjalus, Hybodilla, Sumatrillo and Tuberillo species are often found below the litter layer in the humus or at the soil surface, while Burmoniscus argusticaua is also typical of forested areas [51].

In contrast Redutoniscus, Nagarus and many Burmoniscus species are typically found elsewhere in disturbed sites such as cultivated areas and urban parks (Taiti, unpublished data) often on the surface of the litter, sheltering by day under stones, dead wood or palm leaves, which are habitats typically occupied by more eurydynamic species in temperate regions [61]. They may similarly have a high range of rf values and greater potential to increase their density in response to temporarily favourable conditions characteristic of the more disturbed sites. Such species could respond quickly to conditions favourable to rapid population growth as may appertain in these earlier succession communities where leaf litter from the denser ground layer vegetation dominated by grasses and herbaceous species will have less quantitative chemical defences than that derived from woody species characteristic of closed canopy forest and hence would be of higher quality as a food for isopods [26]. There may also be less species of invertebrate predators on more disturbed forest sites as found for beetles [11] and ants [3]. Species density and abundance of both these groups on the disturbed sites in this study was lower than in the primary forest sites (Jones unpublished data). But although woodlice, particularly small individuals, have a wide range of predators [60], there is no evidence that they regulate populations in a density dependent way in contrast to the clear evidence intra-specific competition for limited high quality foods [24,25,49]. A more appropriate representation of processes determining the effects of disturbance on biodiversity of decomposer communities in tropical forests than the intermediate disturbance hypothesis may be Huston’s elaboration of it in his dynamic equilibrium model [30,31]. This postulates that when rates of disturbance are low but population growth rates are high, diversity may be reduced by competitive exclusion and that when rates of population growth are low and levels of disturbance high, local extinctions reduce diversity. However when disturbance is high but population growth rates are also high (as may be the case in this study where higher quality food resources are available in the most disturbed sites) appropriately adapted species can recover from the disturbance and persist in the community. According to this model maximum diversity occurs where there is a balance between competitive exclusion and disturbance [48]. Thus an undisturbed community with slow growing populations, e.g. primary forests with low quality foods, may have a similar diversity

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to a community containing rapidly growing populations located in areas of high disturbance, e.g. sites such as the orchard and oil palm plantation where well developed ground layer vegetation provides high quality leaf litter. The predictions of this model are thus supported more strongly by our observations than the predictions of the simpler intermediate disturbance hypothesis. While there were no significant differences in diversity of the isopod fauna between disturbed and corresponding undisturbed habitats, there were significantly more species (on average more than double the number) at the two Danum Valley sites than at the other three sites. Studies of termites, ants, beetles and earthworms at Danum Valley and Sepilok suggest that for these groups the effects of forest fragment size are very important in influencing species richness of these members of the soil fauna ([3], Eggelton and Jones, unpublished data). The primary forest at Danum Valley is 10 times bigger than the primary forest at Sepilok and the logged forest at Danum is part of a very much larger logged secondary regrowth area. If this is part of the reason for the differences between the two locations it suggests that forest fragmentation may also have an important effect on the biodiversity of these soil arthropods.

[3]

[4]

[5]

[6]

[7]

[8] [9]

[10]

[11]

Acknowledgements We thank the Royal Society of London for travel grants awarded to M.H. and Z.L. and for provision of Laboratory facilities at Danum Valley Field Centre and Dr. Glen Reynolds for his support at the Centre. We are grateful to the Darwin Initiative (UK Government) for support under the ‘Tools for Monitoring Soil Biodiversity in the ASEAN Region’; The Tropical Biology and Conservation Institute, The University of Malaysia Sabah for support for Z.L.; Dr. Arthur Y.C. Chung for assistance with logistical arrangements and for details of some of the sampling sites and Danum Valley Scientific Committee for permission to work in the Danum Valley Conservation Area. This paper is No. A/426 of the Royal Society of London SE Asia Rainforest

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