Diversity of Pselaphine Beetles (Coleoptera: Staphylinidae: Pselaphinae) in Eastern Thailand

Entomological Science (2008) 11, 301–313 doi:10.1111/j.1479-8298.2008.00281.x

ORIGINAL ARTICLE

Diversity of pselaphine beetles (Coleoptera: Staphylinidae: Pselaphinae) in eastern Thailand

Watana SAKCHOOWONG1,2, Shûhei NOMURA3, Kazuo OGATA4 and Jariya CHANPAISAENG1 1Department of Entomology, Faculty of Agriculture, Kasetsart University, 2National Parks, Wildlife and Plant Conservation Department, Bangkok, Thailand; 3Department of Zoology, National Museum of Nature and Science, Tokyo, and 4Institute of Tropical Agriculture, Kyushu University, Fukuoka, Japan

Abstract Pselaphine beetles (Coleoptera: Staphylinidae: Pselaphinae) are cosmopolitan, species-rich, and yet poorly studied, particularly in the tropics. We sampled beetles in three types of primary forest and two types of disturbed forest habitats in eastern Thailand to assess the utility of pselaphine beetles as bioindicators of forest disturbance. We simultaneously measured leaf litter mass, soil moisture, soil acidity and canopy cover at each site to infer which environmental factors affect pselaphine beetle diversity and abundance. At each site, pselaphine beetles were extracted from ten 1 m2 samples of leaf litter and soil with Tullgren funnels. We sampled 1867 adult beetles representing six supertribes, 51 genera and 114 morphospecies; 7% of the genera and 92% of the species were undescribed. Forest types differed signiﬁcantly in species richness, abundance, diversity and evenness. Primary forest had greater numbers of species and individuals, and higher diversity indices (H′). Teak plantation and secondary forest had substantially fewer individuals and species of pselaphine beetles. Species composition differed between primary and degraded forests. Canopy cover, soil moisture, and leaf litter mass positively correlated with beetle species richness and abundance. Leaf litter mass and soil moisture were the two most important factors affecting the diversity of pselaphine beetle assemblages. Among the 114 morphospecies collected, 43 morphospecies were speciﬁc to two or three habitats and 64 morphospecies were found only in a single habitat. Thus pselaphine beetles appear to have rather narrow habitat requirements and their presence/absence was correlated with environmental differences. These traits make pselaphine beetles a suitable bioindicator taxon for assessing forest litter diversity and monitoring habitat change. Key words: biodiversity, habitat monitoring, indicator species, litter-dwelling beetle, South-East Asia.

INTRODUCTION and contribute valuable data to studies of comparative biodiversity and conservation (Stork 1988; Coddington Forest-litter-inhabiting arthropods are poorly under- et al. 1997). Pselaphine beetles (Coleoptera: Staphylin- stood because of their small size and complex habitats. idae: Pselaphinae) are among the most species-rich However, they play an essential role in nutrient cycling forest-litter-inhabiting group (Carlton 1999). They are also commonly known as ant-like litter beetles or short- winged mold beetles (Newton & Chandler 1989; Triple- horn & Johnson 2005) and are not economically Correspondence: Watana Sakchoowong, Forest Entomology important as pests, but play an important role in the soil and Microbiology Group, National Parks, Wildlife and Plant Conservation Department, 60 Praholyothin Road, ecosystem as predators of small invertebrates (Newton Chatuchak, Bangkok 10900, Thailand. & Chandler 1989). This subfamily is species-rich and Email: [email protected] cosmopolitan, and pselaphine beetles might therefore Received 11 January 2008; accepted 20 May 2008. be proﬁtably used as indicator species for identifying

Figure 1 Map showing the study sites in the eastern forest complex, Thailand, consisting of Khao Ang Rue Nai Wild- life sanctuary (KARN) where the habitats are primary mixed deciduous forest (PMDF) and secondary mixed deciduous forest (SMDF); Khao Sao Dao Wildlife sanctuary (KSD) where the habitats are moist evergreen forest (MEF) and teak plantation (TP); and Khao Kitchakut National Park (KKK) where the habitat is hill evergreen forest (HEF). habitat differences (Carlton 1999) and lack of distur- tuary (KSD) with a total area of 744.58 km2, and the bance in old-growth forests (Newton & Chandler Khao Kitchakut National Park (KKK) with a total area 1989). of 58.31 km2. Precipitation in KARN is blocked by high Although these beetles are diverse in the tropics, most mountains in KSD, which create a rain shadow, making of the 8400 described species are known from the tem- the KARN climate drier than that at KSD and KKK. perate zones (Newton & Chandler 1989; Carlton 1999), Annual precipitation is approximately 1600 mm at and their ecology has rarely been studied. Several studies KARN and 3800 mm at KSD. In eastern Thailand, the have revealed that pselaphine beetles are among the dry season lasts from November to March and the wet most diverse groups of beetles in leaf litter samples season lasts from May to October (Table 1; Thailand (Carton & Robinson 1998; Chung et al. 2000; Carlton Meteorological Department 2007). Differences in et al. 2004). The biology of pselaphine beetles, particu- precipitation and altitude, which ranges from 100 to larly the patterns of species distributions and commu- 1675 m a.s.l. in the study area, produce three different nity dynamics, has not been studied. Pselaphine beetles forest types (Kasetsart University 2007): mixed decidu- are efficiently collected with simple extraction methods ous forest, moist evergreen forest and hill evergreen (Berlese and Tullgren funnels), and they are readily iden- forest. To investigate the impact of human disturbance tified to genus level by using an identification guide on the local diversity of pselaphine beetles, we chose two to Asian pselaphine genera (S. Nomura, unpublished anthropogenically modified forest types for sampling: identification guide to subfamilies Protopselaphinae and secondary mixed deciduous forest and teak plantation Pselaphinae of Asia (Staphylinidae: Protopselaphinae; (Tectona grandis L.). The forest types are described in Pselaphinae), 2006; Chandler 2001). detail below. To examine whether pselaphine beetles might be useful as indicators of forest disturbance, we examined Primary mixed deciduous forest species diversity and abundance in five forest habitat The primary mixed deciduous forest (PMDF) was domi- types in eastern Thailand and determined which species nated by Lagerstroemia venusta Wall., Lagerstroemia indicate forest habitat type. cuspidata Wall., Pterocarpus macrocarpus Kurz, Sur- egada multiflorum (A. Juss.) Baill. and Syzygium perga- MATERIALS AND METHODS mentaceum (King) P. Chantar. & J. Parn. A PMDF site was established in the Lum Jang Wat subdistrict in Study sites KARN at 13°16′25″N, 101°44′44″E, 155 m a.s.l. The eastern forest complex of Thailand (Fig. 1) consists of two wildlife sanctuaries and one national park: the Moist evergreen forest Khao Ang Rue Nai Wildlife Sanctuary (KARN) with a A moist evergreen forest (MEF) site was established in total area of 1030 km2, the Khao Soi Dao Wildlife Sanc- the Ban Thung Krang subdistrict at 13°01′08″N,

Table 1 Climatic and microenvironmental variables in the study sites in eastern Thailand in 2006 DWD Site Climatic variables January March May July September November KARN Rainfall (mm) 0 101.2 220.5 193.6 404.0 9.0 Humidity (%) 60.5 64.5 65.0 68.0 71.5 54.0 Temperature (°C) 26.6 29.5 29.1 28.7 28.0 28.1 KSD and KKK Rainfall (mm) 2.0 24.9 583.4 705.9 559.1 40.3 Humidity (%) 67.0 75.0 74.5 81.5 80.0 67.0 Temperature (°C) 26.6 28.4 28.4 27.8 27.5 28.2 Site/Forest type Microenvironmental variables KARN/PMDF Soil moisture (%) 10.0 8.0 20.6 18.4 22.3 11.7 Soil acidity (pH) 6.5 6.8 6.7 6.9 6.4 6.1 Canopy cover (%) 95.9 94.6 95.2 96.9 92.8 95.4 Litter wet mass (kg) 1.6 1.4 1.4 2.4 1.8 1.9 KARN/SMDF Soil moisture (%) 8.0 7.8 28.7 28.7 16.6 7.4 Soil acidity (pH) 6.7 6.7 7.0 6.4 6.4 6.9 Canopy cover (%) 84.2 89.4 88.4 91.7 86.8 83.9 Litter wet mass (kg) 0.6 1.2 0.9 1.3 1.1 0.8 KSD/MEF Soil moisture (%) 15.0 10.7 48.5 44.5 35.9 18.5 Soil acidity (pH) 6.2 6.3 6.7 6.6 6.4 6.4 Canopy cover (%) 93.6 92.3 93.7 94.6 92.5 89.9 Litter wet mass (kg) 2.3 1.5 1.6 2.1 2.4 3.0 KSD/TP Soil moisture (%) 9.1 8.0 40.8 25.9 15.7 9.6 Soil acidity (pH) 6.1 6.3 6.4 6.3 6.1 6.3 Canopy cover (%) 39.4 37.0 86.8 80.8 88.4 50.5 Litter wet mass (kg) 0.9 0.8 0.7 0.9 1.2 1.4 KKK/HEF Soil moisture (%) 22.0 25.9 52.3 47.6 35.9 21.5 Soil acidity (pH) 5.9 5.8 5.7 5.9 6.1 5.8 Canopy cover (%) 86.6 94.6 93.6 92.3 89.9 92.6 Litter wet mass (kg) 1.4 2.1 0.9 1.6 1.5 2.6 KARN, Khao Ang Rue Nai Wildlife Sanctuary; KSD, Khao Soi Dao Wildlife Sanctuary; KKK, Khao Kitchakut National Park; PMDF, primary mixed deciduous forest; SMDF, secondary mixed deciduous forest; MEF, moist evergreen forest; HEF, hill evergreen forest; TP, teak plantation; D, dry season; W, wet season (Thailand Meteorological Department 2007).

102°12′46″E, 329 m a.s.l. The dominant tree species The Royal Forest Department has since relocated the were Dipterocarpus alatus Roxb., Mallotus peltatus villages and restored the forest in these areas, which has Muell. Arg., Shorea guiso Blume, Strombosia javanica been recovering for approximately 15 years. At the time Blume and Diospyros transitoria Bakh. of sampling, most of the areas once affected by agriculture and human settlement were covered with vegeta- Hill evergreen forest tion, and some of these areas were approaching an A hill evergreen forest (HEF) site was established at advanced stage of secondary forest; trees were approxi- Khao Prabad at 12°50′14″N, 102°10′20″E, 1069 m mately 10–12 m apart with diameters of 8–15 cm. We a.s.l. The most abundant tree species in HEF were sampled a secondary mixed deciduous forest (SMDF) Scaphium scaphigerum (G. Don) Guib & Planch, site in the Phuthai subdistrict at 13°24′56″N, Castanopsis piriformis Hickel & A. Camus, Archiden- 101°52′53″E, 101 m a.s.l. The most abundant tree dron quocense (Pierre) I. Nielsen and Horsﬁeldia glabra species were S. multiﬂorum, L. venusta, S. pergamenta- (Blume) Warb. ceum and P. macrocarpus. Secondary mixed deciduous forest Teak plantation Human settlements and agriculture disturbed 30% of Teak plantations (TP; Tectona grandis L.) were estab- the land area in the northern part of KARN in 1992. lished along the western boundary of KSD between

1969 and 1992 by the Soi Dao Seed Orchard Station Sorting and identification under the Royal Forest Department project (Soi Dao The samples were taken to the laboratory and psela- Forest Seed Orchard Station 1992). The plantations phine beetles were separated and stored in 80% ethanol. cover 376 ha and have been designated for research and Specimens were identified to genus using the keys of S. economic use. All teak plantations connect to form one Nomura (S. Nomura, unpublished identification guide large monocultural habitat in the KSD region. The teak on subfamilies Protopselaphinae and Pselaphinae of ′ ″ ′ ″ plantation site (12°58 48 N, 102°17 49 E, 202 m a.s.l.) Asia (Staphylinidae: Protopselaphinae; Pselaphinae), chosen for this study was located within a 20 ha area 2006), which adopt the taxonomic conventions of planted in 1976, with trees spaced 6 m apart. The Newton and Thayer (1995) and Chandler (2001). After average diameter of teak trees was 30 cm and the generic identification, specimens were then identified to average height was 25 m. Other tree species in the study morphospecies based on the external characteristics of site were Parkia sumatrana Miq., P. macrocarpus, specimens – a technique commonly used as a surrogate Lepisanthes rubiginosa (Roxb.) Leenh. and Dalbergia for species-level identification in biodiversity studies nigrescens Kurz. (Abbott et al. 2002). Voucher specimens were mounted, Sampling methods labeled and deposited in the Museum of Nature and Science Tokyo (MNST) in Japan, the Insect Museum of 2 Ten 1 m quadrats were randomly sampled in each plot. the Department of Entomology at Kasetsart University, The litter and surface soil to a depth of 3 cm was Bangkok, Thailand and the Forest Insect Museum, scraped from the ground and sifted through a 1 cm wire Department of National Parks, Wildlife and Plant mesh sieve to exclude larger debris. After sifting, each Conservation, Bangkok, Thailand. sample was transferred to a debris bag for transporta- tion to the field station where Tullgren funnels were set Data analysis up. At the field station, the contents of each debris bag Data on the number of beetle individuals and species were weighed and divided into ten samples, then put in from ten quadrats in each sampling period were pooled Tullgren funnels for extraction. Soil- and litter-dwelling for analysis. The Shannon diversity index (H′) was cal- organisms were extracted over 48 h using 60 W incan- culated to measure diversity within habitats (Magurran descent lights. Specimens were preserved in 80% 1988) using the formula H′ =-Spi ln pi, where pi is the ethanol prior to processing. Collections were conducted proportional abundance of the ith species = (ni/N). in January, March, May, July, September and November Pielou’s evenness index (J′) was used to quantify dif- 2006. ferences in relative abundance using the formula J′ = H′/ln S, where S is the number of species (Ludwig & Weather and microenvironmental data Reynolds 1988). Monthly rainfall, relative humidity, and temperature Kruskal–Wallis tests were used to assess differences in data were obtained from the Thailand Meteorological beetle species richness, number of individuals, the Department. All data were collected by the provin- Shannon diversity index (H′) and Pielou evenness index cial meteorological stations located in Chachoengsao, ( J′) among habitats, and Mann–Whitney U-tests were KARN and Chanthaburi, KSD and KKK (Thailand performed to examine the differences in beetle species Meteorological Department 2007). Microenvironmen- richness, number of individuals, Shannon diversity tal variables were measured to investigate their rela- index (H′) and Pielou evenness index ( J′) between dry tionship with species presence and abundance, and and wet seasons. percentage canopy cover was measured with a spherical Multiple regression and Pearson’s correlation analysis densitometer. Percentage soil moisture was calculated by were used to determine which environmental variables comparing the wet and dry weights of soil samples col- were related to species richness and abundance. All non- lected with a core sampler 5 cm long and 5 cm in diam- parametric tests, regression and Pearson’s correlation eter. Ten samples were taken from each site by driving analysis were performed with Systat Version 8 (Systat the core sampler into the ground in the middle of a 1 m2 Software 1998). sampling area. The samples were weighed then dried in To assess the similarity of beetle communities among an oven until the weight remained constant. After forest types, Sørensen similarity indices (QS) were cal- sifting, leaf litter mass was measured in the field. Each of culated using binary presence/absence data for psela- these environmental variables was measured when a phine beetles in each sample with the formula QS = 2c/ sample was collected (Table 1). (a + b), where a is the number of species in sample a; b

is the number of species in sample b; and c is the number of species found in both samples (Wolda 1981). Detrended correspondence analysis (DCA) was also used to determine the similarity of pselaphine assemblages using species richness and abundance data (Hill & Gauch 1980). Species sampled fewer than three times were excluded, because rare species may misrepresent the overall species composition of a habitat. Thus, only 48 species were included in the DCA analysis. Data on individuals were down-weighted in proportion to their frequency. Axes were rescaled with a threshold of zero, and the number of segments was set to the default value of 26. Indicator species analysis (ISA) was performed using the technique of Dufrene and Legendre (1997) with a signiﬁcance level of P Յ 0.01, as proposed by these Figure 2 Pselaphine species richness in sampling sites in Ϯ authors. Detrended correspondence analysis and ISA eastern Thailand. Bars show mean SE (n = 3). See Figure 1 for abbreviations of forest habitats. (ᮀ), Dry season; (᭿), wet were performed using PC-ORD 4.27 (McCune & season. Mefford 1999).

RESULTS sp. 1, Morana sp. 1 and Aphilia sp. 1. At the other end In total, we sampled 1867 pselaphine beetle adults, re- of the abundance spectrum, 30 species (26% of the presenting six supertribes and 114 morphospecies. total) were represented by two or three individuals, These species could be assigned to 51 described genera and 29 species (25% of total) were represented by one and several undescribed genera. Most of them were in individual. the supertribe Bythinoplectitae. One hundred and five Species richness species out of the 114 were apparently undescribed. Nine species could be identified by comparison with Pselaphine beetle diversity among habitats was nega- the type specimens preserved in the Muséum National tively related to the degree of disturbance, and was d’Histoire Naturelle, Paris, France (MHNP). In this several times higher in the three primary forest habitats study, we found three species of the genus Articerodes than in the secondary forest and teak plantation. Alpha that were recently described by Nomura et al. (2008). diversity among habitats varied in the following way: Species in the supertribe Goniaceritae were numerically MEF (66 species) > MDF and HEF (42 each) > SMDF dominant, comprising 919 individuals (49%) and 29 (23) > TP (21; Appendix I). The mean number of psela- species (25%) of the total collection, and the Goniaceri- phine beetle species significantly decreased from moist tae were the dominant group in every forest habitat. The undisturbed MEF to teak plantation (Kruskal–Wallis second most diverse supertribe was the Euplectitae, with test; H = 18.51, P = 0.001, d.f. = 4; Fig. 2). Pselaphine 29 species (25%) and 295 individuals (14%), followed beetle communities were more species rich in the wet by the Batrisitae with 18 species (16%) and 363 indi- season than in the dry season, particularly in PMDF, viduals (9%), the Bythiniplectitae with 18 species (16%) SMDF and TP, but this trend was marginally non- and 109 individuals (6%), the Pselaphitae with 16 significant when data from all sites were combined species (13%) and 193 individuals (10%), and the Clav- (Mann–Whitney U-test, U = 70.50, P = 0.08, d.f. = 1). igeritae with four species (3%) and 24 individuals (1%). The six most abundant species present in all habitats Abundance accounted for approximately 58% (1086 of 1867) of the Pselaphine abundance was also significantly greater in total individuals. Plagiophorus sp. 1 in the supertribe primary forests than in the secondary forest and teak Goniaceritae was the most abundant species, repre- plantation (H = 23.04, P = 0.01, d.f. = 4; Fig. 3). The sented by 431 individuals or 23% of the pselaphine number of individuals in primary forest habitats, par- beetles counted. Mnia sp. 1 represented 13%, Batraxis ticularly PMDF and MEF, was several times higher than doriae represented 10%, followed by Centrophthalmus in disturbed forest habitats. However, the number of

Figure 3 Abundance (log10) of pselaphine beetles in ﬁve differ- Figure 4 Shannon’s diversity indices (H′) for pselaphine ent forest habitats in eastern Thailand. Bars show mean Ϯ SE beetles in ﬁve different forest habitats in eastern Thailand. Bars (n = 3). See Figure 1 for abbreviations of forest habitats. (ᮀ), show mean Ϯ SE (n = 3). See Figure 1 for abbreviations of Dry season; (᭿), wet season. forest habitats. (ᮀ), Dry season; (᭿), wet season.

beetles captured in HEF was not as high as the number of beetles collected in PMDF and MEF. When data from all sites were combined, seasonal differences in abundance were not signiﬁcant (U = 82, P = 0.2, d.f. = 1).

Shannon diversity (HЈ) and Pielou evenness ( JЈ) indices Shannon diversity indices (H′) were higher in primary forest habitats than in disturbed habitats. Moist evergreen forest had the highest diversity, and diversity decreased from HEF to TP (Fig. 4). There were significant differences in Shannon diversity indices among habitats (H = 13.35, P = 0.01, d.f. = 4), but seasonal differences in Shannon diversity indices were marginally Figure 5 Pielou’s evenness indices ( J′) for pselaphine beetles in non-significant when data from all sites were combined five different forest habitats in eastern Thailand. Bars show (U = 70, P = 0.07, d.f. = 1). mean Ϯ SE (n = 3). See Figure 1 for abbreviations of forest ᮀ ᭿ In contrast, Pielou evenness indices (J′), which quan- habitats. ( ), Dry season; ( ), wet season. tify the relative abundance of species in each habitat, showed that beetle communities in disturbed habitats such as TP and SMDF were more even than those sity (H′) U = 31, P = 0.40; evenness ( J′), U = 50, in primary forests (H = 10.21, P = 0.03, d.f. = 4). Again, P = 0.40; all d.f. = 1). However, most parameters seasonal differences in evenness were not significant differed significantly between dry and wet seasons in (U = 111.5, P = 0.77, d.f. = 1; Fig. 5). degraded habitats (SMDF and TP), except Pielou When data from primary forests habitats (PMDF, evenness (J′) indices (species richness, U = 3, P = 0.01; MEF and HEF) were pooled and analyzed separately abundance, U = 5, P = 0.03; H′, U = 3, P = 0.01; J′, from pooled data from degraded forests (SMDF and U = 18, P = 1.00; all d.f. = 1). TP), we found no significant differences in species richness, abundance, diversity or evenness between dry Species composition differences and wet seasons in primary forests (species richness, Sørensen similarity indices (QS) revealed that samples U = 23.5, P = 0.13; abundance, U = 25, P = 0.17; diver- collected in MEF and MDF sites had similar species

Table 2 Similarity matrix of the pselaphine species composition in the ﬁve forest habitats in eastern Thailand PMDF HEF MEF SMDF TP PMDF – 13 27 9 9 HEF 0.31 – 17 8 8 MEF 0.50 0.31 – 14 8 SMDF 0.28 0.25 0.32 – 8 TP 0.28 0.25 0.21 0.37 – Numbers in the upper right half of the table are the number of species shared between each site, and numbers in the lower left half are the indices of similarity (Sørensen index, QS). See Figure 1 for abbreviations of forest habitats.

assemblages, with a value of 0.50. HEF had a QS of 0.31, as did MDF and MEF. Secondary mixed deciduous forest and TP both had a QS of 0.37. Differences in QS between all primary forests and SMDF or TP ranged from 0.21 to 0.32 (Table 2). Figure 6 Detrended correspondence analysis for pselaphine Site differences were also evident in the DCA ordina- beetles in sampling sites in eastern Thailand. See Figure 1 for tion plot. Axis 1 (eigenvalue 0.68) grouped composition abbreviations of forest habitats. among plots, while axis 2 (eigenvalue 0.49) separated composition between the primary forests and degraded forests. Three distinct groups of pselaphine beetle Some environmental variables were significantly assemblages were clustered into: (i) primary forest correlated with the species richness and abundance of groups comprising PMDF and MEF; (ii) HEF; and (iii) pselaphine beetles (Table 5). Leaf litter mass was most degraded forest habitats (SMDF and TP) (Fig. 6). strongly correlated with species diversity (r = 0.724) and abundance (r = 0.705). Soil moisture and canopy cover Indicator species analysis were correlated with species richness (r = 0.379 and In indicator species analysis, data on the frequency and 0.397, respectively) but not with abundance. Regression relative abundance of species in a particular habitat are analysis (figure not shown) showed that leaf litter mass examined simultaneously. The significance of the indi- was the most important variable determining the cator was tested by generating a null distribution with presence of pselaphine beetles, accounting for 52% 2 Monte-Carlo randomization. Moist evergreen forest (r = 0.524; F1,27 = 26.72, P < 0.01) and 50% of the 2 had the greatest number of indicator species, followed variation in abundance (r = 0.497; F1,27 = 26.72, by PMDF and then HEF. Teak plantation had one indi- P < 0.01). Soil moisture and canopy cover only 2 cator species, while no indicator species were found in accounted for 14% (r = 0.144) (F1,27 = 4.54, P < 0.05) SMDF (Table 3). and 16% of the variation in species richness (r2 = 0.158

(F1,27 = 5.061, P < 0.05), respectively. Microenvironmental variables related to species richness and abundance DISCUSSION Climate and microenvironment data are given in Table 1. There were significant differences among the Most of the collected specimens are undescribed species microenvironmental variables in different forest habitats and some are undescribed genera. In the tropics, psela- (Table 4). Primary forests had greater soil moisture, phine beetles are one of the most diverse taxa, in which canopy cover and leaf litter than the secondary forest or most species have not been formally described (Carlton teak plantation. However, soil acidity (pH) in HEF was 1999). In Thailand, fewer than 40 species have been lower than that at other sites (pH = 5.9). Secondary recorded in this group, most of which were collected mixed evergreen forest had significantly less litter and in Bangkok and surrounding areas from the 19th soil moisture, whereas TP had significantly less litter and century (Motschulsky 1851; Schaufuss 1877; Raffray soil moisture and a lower level of canopy cover. 1904a,b; Hlavac 2002). Only 8% of the total number of

Table 3 Result of indicator species analysis Forest habitat/species Supertribe Indicator value (%) P < 0.01 PMDF Bythinoplectina gen. undet. sp. 3 Bythinoplectitae 60.0 0.008 Hypochareus sp. 1 Batrisitae 38.3 0.004 Tribasodites sp. 3 Batrisitae 42.9 0.004 Harmophorus sp. 2 Goniaceritae 83.3 0.002 Plagiophorus sp. 1 Goniaceritae 83.3 0.001 Centrophthalmus sp. 1 Pselaphitae 73.0 0.001 HEF Leptoplectus sp. 1 Euplectitae 46.7 0.004 Cerylambus reticulatus Clavigeritae 60.6 0.01 Tmesiphorus sp. 2 Pselaphitae 50.0 0.002 MEF Batriscenaulax sp. 1 Batrisitae 45.8 0.001 Mnia sp. 1 Batrisitae 89.0 0.001 Aphilia sp. 1 Euplectitae 44.0 0.005 Bibloplectus sp. 1 Euplectitae 50.0 0.002 Euplectodina sp. 1 Euplectitae 57.6 0.002 Pseudoplectus sp. 4 Euplectitae 46.4 0.003 Prophilus sp. 1 Euplectitae 63.5 0.004 Harmophorus sp. 1 Goniaceritae 68.3 0.001 Atenisodus sp. 1 Goniaceritae 66.0 0.003 Comatopselaphus puncticollis Goniaceritae 50.0 0.003 Batraxis doriae Goniaceritae 48.9 0.002 Batraxis brevis Goniaceritae 66.7 0.002 Morana sp. 1 Goniaceritae 50.0 0.002 Ancystrocerus sp. 1 Pselaphitae 83.3 0.001 Pseudophanias sp. 1 Pselaphitae 86.7 0.002 TP Parapyxidicerus sp. 1 Bythinoplectitae 60.0 0.007 See Figure 1 for abbreviations of forest habitats. No indicator species were found for SMDF.

Table 4 Two-way anova of microenvironmental variables in different forest habitats in eastern Thailand F-ratio Source of variation d.f. Soil moisture (%) Soil acidity (pH) Canopy cover (%) Litter wet mass (kg) Habitat 4 16.97** 14.51** 86.29** 8.33** Season 1 80.24** 0.97 61.15** 0.55 Habitat ¥ Season 4 2.96* 1.02 46.08** 1.06 *<0.05, **<0.01. morphologically distinguishable species were identifi- Species richness, abundance and diversity values were able to named species. Difficulties in assigning species to several times higher in primary forests (MEF, PMDF genera were most pervasive within the supertribe Bythi- and HEF) than in secondary forests or teak plantation noplectitae. Undescribed species and genera from this (Figs 2–4). This is not surprising, as pselaphine study will be described in separate taxonomic works. beetles inhabit moist habitats under leaf litter (Chan- dler 2001). Secondary forest and teak plantation Effects of habitat types and had lower soil moisture and less leaf litter than seasonal differences primary forest, resulting in a smaller number of Significant differences in species richness, abundance pselaphine beetle species, and lower abundance and and diversity were found among forest habitats. diversity.

Table 5 Pearson’s correlation coefﬁcients (r) between species richness, abundance of pselaphine beetles and the environmental variables in two different climatic conditions All sites KARN KSD and KKK Environmental variables Species Abundance Species Abundance Species Abundance Soil moisture 0.379* 0.116 0.772** 0.6564* 0.221 0.91 Soil pH 0.77 0.117 -0.51 -0.30 0.515* 0.444* Canopy cover 0.397* 0.279 0.414 0.492 0.520* 0.291 Leaf litter 0.724** 0.705** 0.714** 0.768** 0.707** 0.696** Precipitation 0.234 0.115 0.561* 0.492 0.82 0.11 *<0.05, **<0.01. See Figure 1 for abbreviations of forest habitats.

There were no significant differences in species rich- primary forests (Fig. 6). The ordination in Figure 6 ness, abundance, diversity or evenness between seasons. grouped SMDF2 with primary forest sites. This was due However, the effect of increased rainfall in the wet to the high abundance of Centrophthalmus sp. 1 col- season increased soil moisture more markedly in lected in the second sample from an SMDF plot. Cen- degraded forests (SMDF and TP) than in undisturbed trophthalmus sp. 1 was an abundant species designated forests (MEF, PMDF and HEF). Thus, human distur- as an indicator species of PMDF, but it was occasionally bance increased moisture loss from previously forested collected in SMDF. These high numbers of Centro- areas. The severity of the dry season is regarded as the phthalmus sp. 1 caused the DCA analysis to group the most significant factor determining a species’ ability to SMDF2 sample with samples from PMDF and MEF. survive in a tropical forest (Whitmore 1998), and the The SMDF4 sample did not group near any other clus- depressed species diversity in disturbed forests may very ters in the detrended correspondence analysis (Fig. 6). well result from this effect of increasing the severity of Two of the most abundant species in this sample, Pareu- the dry season. plectops sp. 1 and Parapyxidicerus sp. 1, were found in Species richness and diversity (H′) clearly increased in several different habitat types. One individual of Pareu- secondary forest and the teak plantation in the wet plectops sp. 1 was collected in each of the following season (Figs 2,4). Interestingly, secondary forest and the forest types: PMDF, HEF, MEF and SMDF, and approxi- teak plantation had higher values of the evenness index mately equal numbers of Parapyxidicerus sp. 1 were (J′) than did the primary forests. This indicates that collected from PMDF (three individuals), MEF (three), natural forests have higher diversity, while disturbed and SMDF (two). The abundance of these habitat- forests are more spatially homogenous. Primary forests generalist beetle species within the SMDF4 sample is the were home to a greater number of species, resulting in most likely explanation for its position as an outlying higher diversity value (H′), but a few dominant species, point in the DCA ordination (Fig. 6). for example Plagiophorus sp. 1, Harmophorus sp. 1 and Centrophthalmus sp. 1, were all common in samples Indicator species of habitat types from PMDF, and its evenness index was therefore lower Indicator species respond to environmental differences than those of SMDF and TP. among habitat types, and their presence therefore indicates the overall diversity and complexity of an assem- Species composition blage (Samways 2005). Many beetle groups have been Pselaphine communities were most similar (QS = 0.50) used as indicators, including dung beetles, ground in the two primary forest types (PMDF: MEF). Interest- beetles, and curculionid beetles (Goehring et al. 2002; ingly, although both TP and SMDF were connected to Larsen & Work 2003; Ødegaard 2006). Taxonomic primary forest at our sites, each had fewer species and impediments not withstanding, pselaphine beetles have individuals than the primary forest. Species assemblages many benefits for use as indicator species (New 1998): of SMDF and TP had a higher proportion of shared they live in a defined habitat (forest litter), respond to species (QS = 0.37) than did any pairs of primary and environmental changes, and can be easily sampled. disturbed forests (Table 2). Species richness and abundance of pselaphine beetles Detrended correspondence analysis separated psela- responded to habitat change in a consistent manner: phine communities in SMDF and TP from those of the both declined along a forest disturbance gradient.

Notably, the greatest number of indicator species was because humidity and other environmental variables found in MEF, followed by PMDF and HEF. Teak plan- were lower in disturbed areas, a result that echoes many tations had only one indicator, and SMDF had no indi- other reports that species richness of vertebrate and cator species (Table 3). Pselaphine beetles are usually invertebrate faunas generally decline with increasing dis- habitat-specific. Our study showed that only two of the turbance (Lawton et al. 1998; Jones et al. 2003; Harvey 114 species were found in all habitats, and only seven & Gonzalez 2006). species were found in four habitats. Forty-three species were found to be specific to two or three habitats, and ACKNOWLEDGMENTS 64 species were found in only one habitat (Appendix I). This work was supported by the Thailand Research Microenvironmental variables related to Fund through the Royal Golden Jubilee PhD program pselaphine assemblages (grant no. PHD/0154/2547). We thank Mr Yu Sen- Microenvironmental variables were apparently signifi- atham, the superintendent of Khao Ang Rue Nai Wild- cantly less variable in secondary forest and teak planta- life Sanctuary, Mr Sawai Wanghongsa, the chief of tion sites compared with the three primary forest sites Khao Ang Rue Nai Wildlife Research Station, Mr (Tables 1,4). Leaf litter mass was strongly correlated Surachai Pransil, the superintendent of Khao Kitchakut with species richness (r = 0.724) and abundance National Park for their support and provisioning of field (r = 0.705; Table 5) for all sites, and was also strongly work, Mr Sungwon Ratanachan, the chief of the Forest correlated with species diversity and abundance in all Entomology Research Center in Chanthaburi who plots in KARN and KSD. Only litter mass affected beetle kindly offered accommodation during our field work, abundance (Table 5). Precipitation and soil moisture Dr David Lohman from the National University of Sin- were correlated with species richness in KARN. On the gapore and Dr Weerawan Amornsak from Kaseetsart other hand, precipitation and soil moisture did not cor- University who provided valuable comments on earlier relate with species richness in KSD. This was not sur- drafts of the manuscript. Permission to collect the prising, as the sites in KARN that had less precipitation samples for this project was granted by the National were more influenced by the rainy season, but in KSD, Parks, Wildlife and Plant Conservation Department, higher year-round rainfall increased relative humidity, Thailand. accounting for the lack of correlation between species richness and season. Thus, the results indicate that REFERENCES the most important factors for pselaphine beetle assemblages are leaf litter and soil moisture. Abbott I, Burbidge T, Strehlow K, Mellican A, Wills A (2002) Normally, the environments in the primary forests, Logging and burning impacts on cockroaches, crickets degraded forest (SMDF), and monoculture teak planta- and grasshoppers and spiders in Jarrah Forest, Western tion are qualitatively very different, which thus could Australia. Forest Ecology And Management 174, 383– 399. potentially influence pselaphine species richness, abun- Carlton CE (1999) Annotated checklist of Staphylinidae, dance and composition. In disturbed habitats, trees are subfamily Pselaphinae from Rio Bravo Conservation generally smaller with fewer species and the mass of leaf and Management Area, Orange Walk District, Belize. litter is therefore less. The land is more open, which [Cited 18 November 2005.] Available from URL: decreases moisture and leaf litter. These important http://www.agctr.lsu.edu/Inst/Research/Departments/ microclimatic factors may account for the lower diver- arthropodmuseum/belize%20pselaph.htm/ sity of soil-dwelling animals in these perturbed habitats. Carton CE, Robinson HW (1998) Diversity of litter-dwelling Primary forests provide a variety of microhabitats, beetles in the Ouachita Highlands of Arkansas, USA including a diversity of tree species, litter layers, mois- (Insecta: Coleoptera). Biodiversity and Conservation 7, ture gradients, organic matter types and food to provide 1589–1605. Carlton CE, Dean M, Tishechkin A (2004) Diversity of two for the needs of living organisms. Ecosystem diversity is beetle taxa at a Western Amazonian locality (Coleoptera: thus positively related to habitat complexity. Histeridae; Staphylinidae, Pselaphinae). The Coleopterists This study provides the first overview of pselaphine Bulletin 58, 163–170. beetle diversity in the last and largest network of pro- Chandler DS (2001) Biology, Morphology and Systematics of tected areas in eastern Thailand. Species richness and the Ant-like Litter Beetle genera of Australia (Coleoptera: abundance were high in the primary forests and low in Staphylinidae: Pselaphinae). Memoirs on Entomology, the secondary forest and teak plantation presumably Vol. 15. Gainesville, FL.

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APPENDIX I Table A1 Species and individuals of pselaphine beetles collected in ﬁve different forest habitats in eastern Thailand in 2006

Forest habitat Total no. Supertribe Species PMDF SMDF MEF HEF TP individuals

Batrisitae Amana sp. 1 11 2 Batrisitae Batriscenaulax sp. 1 16 21 1 38 Batrisitae Batrisiella sp. 1 13 13 Batrisitae Batrisodes sp. 1 11 Batrisitae Hypochareus sp. 1 7 3 1 1 12 Batrisitae Hypochareus sp. 2 22 Batrisitae Hypochareus sp. 3 1 1 Batrisitae Mnia sp. 1 1 210 25 236 Batrisitae Physomirinus sp. 1 11 Batrisitae Sathytes sp. 1 4 4 Batrisitae Tribasodites sp. 1 13 16 29 Batrisitae Tribasodites sp. 2 3 3 Batrisitae Tribasodites sp. 3 6 1 7 Batrisitae Tribasodites sp. 4 1 1 2 Batrisitae Tribasodites sp. 5 2 4 6 Batrisitae Trisinus sp. 1 2 1 3 Batrisitae Batrisina gen. undet. sp. 1 2 2 Batrisitae Batrisina gen. undet. sp. 2 1 1 Bythiniplectitae Octomicrus longulus 1 1 Bythiniplectitae Parayxidicerinus sp. 1 1 2 1 11 15 Bythiniplectitae Tuberoplectus sp. 1 8 8 Bythiniplectitae Zethopus opacus 2237 Bythiniplectitae Bythinoplectina gen. undet. sp. 1 2 2 4 Bythiniplectitae Bythinoplectina gen. undet. sp. 2 5 5 Bythiniplectitae Bythinoplectina gen. undet. sp. 3 18 2 20 Bythiniplectitae Bythinoplectina gen. undet. sp. 4 11 Bythiniplectitae Pyxidicerina gen. undet. sp. 1 5 6 4 3 18 Bythiniplectitae Pyxidicerina gen. undet. sp. 2 3 5 3 11 Bythiniplectitae Pyxidicerina gen. undet. sp. 3 2 1 3 1 7 Bythiniplectitae Pyxidicerina gen. undet. sp. 4 1 3 4 Bythiniplectitae Pyxidicerina gen. undet. sp. 5 1 1 Bythiniplectitae Pyxidicerina gen. undet. sp. 6 1 1 Bythiniplectitae Pyxidicerina gen. undet. sp. 7 1 1 Bythiniplectitae Pyxidicerina gen. undet. sp. 8 1 1 Bythiniplectitae Pyxidicerina gen. undet. sp. 9 2 2 Bythiniplectitae Pyxidicerina gen. undet. sp. 10 2 2 Clavigeritae Articerodes ohmomoi 2 2 Clavigeritae Articerodes thailandicus 88 Clavigeritae Articerodes jariyae 33 Clavigeritae Cerylambus reticulatus 110 11 Euplectitae Aphilia sp. 1 35 4 46 1 1 87 Euplectitae Bibloporus sp. 1 3 3 Euplectitae Bibloporus sp. 2 3 3 Euplectitae Bibloporus sp. 3 1 1 2 Euplectitae Bibloporus sp. 4 2 2 Euplectitae Bibloporus sp. 5 1 1 Euplectitae Bibloporus sp. 6 11 Euplectitae Bibloplectus sp. 1 8 8 Euplectitae Euplectus sp. 1 1 11 1 13 Euplectitae Euplectus sp. 2 1 2 3 Euplectitae Euplectodina sp. 1 2 19 1 22 Euplectitae Leptoplectus sp. 1 17 1 18 Euplectitae Leptoplectus sp. 2 1 5 6 Euplectitae Leptoplectus sp. 3 55 Euplectitae Leptoplectus sp. 4 11 Euplectitae Philiopsis sp. 1 1 5 1 7 Euplectitae Prophilus sp. 1 1 20 21 Euplectitae Prophilus sp. 2 11 Euplectitae Pseudoplectus sp. 1 1 1 Euplectitae Pseudoplectus sp. 2 1 1 Euplectitae Pseudoplectus sp. 3 1 1 Euplectitae Pseudoplectus sp. 4 1 13 14 Euplectitae Pseudoplectus sp. 5 11

Table A1 Continued

Forest habitat Total no. Supertribe Species PMDF SMDF MEF HEF TP individuals

Euplectitae Pseudoplectus sp. 6 1 1 2 Euplectitae Saulcyella sp. 1 1 1 1 3 Euplectitae Saulcyella sp. 2 11 Euplectitae Saulcyella sp. 3 1 26 27 Euplectitae Saulcyella sp. 4 1 1 2 Euplectitae Panaphantina gen. undet. sp. 1 1 1 2 Goniaceritae Atenisodus sp. 1 3 3 32 2 40 Goniaceritae Atenisodus sp. 2 3 1 4 Goniaceritae Atenisodus sp. 3 22 Goniaceritae Atychodea sp. 1 11 Goniaceritae Batraxis brevis 27 27 Goniaceritae Batraxis doriae 51 140 191 Goniaceritae Batraxis sp. 1 2 2 Goniaceritae Batraxis sp. 2 2 2 Goniaceritae Comatopselaphus punticollis 11 11 Goniaceritae Eupines sp. 1 2 1 3 Goniaceritae Eupines sp. 2 1 1 Goniaceritae Harmophorus gibbiodes 347 Goniaceritae Harmophorus sp. 1 1 31 1 4 37 Goniaceritae Harmophorus sp. 2 16 16 Goniaceritae Harmophorus sp. 3 4 4 Goniaceritae Mechanicus sp. 1 11 Goniaceritae Morana sp. 1 52 52 Goniaceritae Natyplerus sp. 1 8 8 Goniaceritae Pareuplectops sp. 1 1 3 1 1 2 8 Goniaceritae Pareuplectops sp. 2 22 Goniaceritae Plagiophorus sp. 1 359 1 26 45 431 Goniaceritae Plagiophorus sp. 2 6 20 9 35 Goniaceritae Plagiophorus sp. 3 11 Goniaceritae Rybaxis sp. 1 1 1 Goniaceritae Sunorfa sp. 1 2 20 22 Goniaceritae Trissemus sp. 1 2 1 3 Goniaceritae Trissemus sp. 2 1 1 Goniaceritae Trissemus sp. 3 2 1 3 Goniaceritae Natypleurina gen. undet. sp. 1 3 3 Pselaphitae Ancystrocerus sp. 1 8 8 Pselaphitae Apharina conicicollis 88 Pselaphitae Apharina sp. 1 1 1 Pselaphitae Apharinodes sp. 1 22 Pselaphitae Centrophthalmus sp. 1 65 24 89 Pselaphitae Centrophthalmus sp. 2 11 Pselaphitae Hamotopsis sp. 1 4 4 Pselaphitae Labomimus sp. 1 8 3 11 Pselaphitae Labomimus sp. 2 1 4 5 Pselaphitae Labomimus sp. 3 22 Pselaphitae Pselaphidius sp. 1 1 1 Pselaphitae Pselaphodes sp. 1 1 1 2 Pselaphitae Pseudophanias sp. 1 4 26 30 Pselaphitae Tmesiphorus sp. 1 1 12 13 Pselaphitae Tmesiphorus sp. 2 15 15 Pselaphitae Tyraphus pilosus 1 1 Total 646 75 925 187 43 1876 The total number of species found was 114 (42 in PMDF, 23 in SMDF, 66 in MEF, 42 in HEF and 21 in TP). PMDF, primary mixed deciduous forest; SMDF, secondary mixed deciduous forest; MEF, moist evergreen forest; HEF, hill evergreen forest; TP, teak plantation.