Fern Communities in Lowland Tropical Forests of Brunei Darussalam, Borneo: Diversity, Indicator Species, and Environmental Drivers Across Forest Types

Tropical forests undisputedly harbor the largest share of global plant diversity, but the mechanisms of maintenance for this diversity cannot be well understood without good data on environmental variables, primarily soil characteristics. This study investigates differences in soil physico-chemical properties in various tropical lowland forest types in Brunei Darussalam, in the Northwest Borneo plant diversity hotspot. Nine different vegetation types were investigated: intact primary mixed-dipterocarp forest, old disturbed secondary forest, young disturbed secondary forest (partly invaded by alien Acacias), heath (Kerangas) forest, peat swamp forest, swampy heath (Kerapah) forest, core mangrove, fringe mangrove and island mangrove forests. Nine 60 x 20 m plots were set up, and sampled for soils at topsoil (0-15 cm depth) and subsoil (15-30 cm depth) layers. Soil gravimetric water and organic matter content, texture, nutrient concentrations, pH, and salinity were determined. The peat swamp and core mangrove forests recorded highest soil nutrient concentrations. Peat swamp forest had the highest GWC, OM content, total N, and total Ca recorded, whereas the soil in core mangrove forest had higher total P, total Mg, total K, exchangeable Mg, exchangeable Ca, exchangeable K and salinity compared to the other habitat types. These results were also highlighted by the principal component analysis for the soil parameters measured. The most nutrient-poor soils were found in the Kerapah and heath forest sites. The difference between topsoil and subsoil for soil variables were generally not significantly different from each other. The present study has shown that soil physico-chemical properties differ significantly between the nine vegetation types studied, and this may have important implications upon differences seen in plant community compositions in these vegetation types.Keywords: Heath forest, Mangrove forest, Mixed Dipterocarp forest, Peat swamps, Edaphic

There are physiognomically distinctive forest types in lowland tropics reflecting variation in edaphic conditions. Tree saplings that contribute to forest regeneration are expected to show morphological properties in response to forest environment. However, it remains unknown how sapling properties are similar or different across forest types. We examined architectural and functional traits of forest floor saplings across heath, peat swamp, and mixed dipterocarp forests that characterize lowland forests in Kalimantan, Indonesia. Saplings (150-310 cm tall) of 41 species, which represent each forest type, were selected under the canopy of developed forest stands. Among these, we chose one species found in all forest types and two species in heath and peat swamp forests. Significant differences in crown allometries were found across forest types and across species. Saplings in mixed dipterocarp forest had thicker trunk and wider crown at the same sapling height compared to other forests and they had higher specific leaf area, higher mass-based leaf nitrogen content and lower wood density. Heath forest saplings showed lowest leaf nitrogen content and highest wood density. Species with across forest-type distribution showed intra-specific variation in sapling traits, and which was similar to the difference among forest types. We conclude that saplings show morphological response to nutritional and water conditions that characterize forest types.

Data of Dipterocarpaceae species have been extracted from 8 studied plots of 1-ha each, distributed in three types of natural forest in Kalimantan (those were 4 plots in mixed dipterocarps forest, 2 plots in peat swamp forest and 2 plots in heath forest types) for further population analysis. Number of Dipterocarpaceae species in mixed dipterocarps forest type was higher than of in two other forest types, however mean number of individual per species was higher in peat swamp and heath forest types than of in mixed dipterocarps forest type. Some of Dipterocarpaceae species are adapted to heath and peat swamp forest type conditions indicated by the number and distribution of population of the species in both forest types. The higher the population number of juvenile trees 5-10 cm in diameter, the lower population number of mature trees of diameter 50cm up, indicated the higher tree population the higher mortality rate. However, survivorship of tree will higher as the tree diameter higher. Survivorship of trees in mixed dipterocarp forest is higher than of in peat swamp and heath forest types.

Seventeen individual trees of 12 species of Castanopsis, Lithocarpus, and Quercus were studied at 2-4 week intervals for most of a year, and reproductive phenology of numerous other individuals and species was recorded over a 3-year period. Inflorescence primordia were macroscopically visible near the end of the wetter season and anthesis of all flushes occurred in the drier season. There was general synchrony of reproduction among reproducing individuals, but a few trees were sterile throughout the observation period. Some had multiple reproductive flushes at 3-5 week intervals. Anthesis in the drier season by Castanopsis and Lithocarpus, which are entomophilous, maximizes pollination because that is the season of insect population peaks. Quercus is anemophilous and therefore is unaffected by insect population cycles. THE RECENT INCREASE IN KNOWLEDGE OF PHENOLOGY of tropical plants, especially those of the seasonal neotropics (Opler et al. 1976, Bawa 1983, Borchert 1983), is the most significant information to accumulate on tropical phenology. In Borneo and other paleotropical areas that are less seasonal, the phenologies are less understood, although definite seasonal rhythms are known for some tree species (Holttum 1940, 1968; Koriba 1958). According to Whitmore (1975), flowering and fruiting of most lowland Far Eastern tropical trees is periodic but regular and often annual; the Dipterocarpaceae, which are dominant over large areas, are noted for their infrequent but gregarious flowering. In his detailed taxonomic treatment of the Fagaceae of Malaysia, Soepadmo (1972) gave flowering and fruiting months for most species, but no dear patterns of regularity or synchrony emerge from that information. However, such patterns might appear locally. Observers in north-temperate dimates are familiar with the annual synchronous flush of leaves and flowers of Quercus (oak) and Fagus (beech) in the spring and Castanea (chestnut) in the summer; sometimes the fertile flush is followed by one or more sterile flushes. Phenology of the paleotropical Fagaceae is more complex. STUDY AREA AND METHODS In Borneo, the Fagaceae occur from sea level to about 3000 m and the largest number of species is found in the lower montane forests from 1200 to 1800 m elevation. The fagaceous trees are often gregarious in the mountains but are mostly scattered in the lowland forests. The three most extensive forest types in the Sarawak lowlands (our study area), are edaphically determined: mixed dipterocarp forest on silty day soils; semi-xerophilous heath forest on relatively infertile, sandy soils; and peat-swamp forests (Ashton 1965, Richards 1965, Briinig 1973). They contain 14, 21, and 5 fagaceous species, respectively (Briinig 1967). The mixed dipterocarp forest is the tallest, has the most tree species, and has irregular surface physiognomy; the Fagaceae occur as trees of the middle storey. The heath forest and peat-swamp forests are lower, less rich in species, and their canopies are more even (Anderson 1964; Briunig 1970, 1973). In them, the Fagaceae occupy mostly the middle and upper storeys. There is little seasonal temperature variation in the Kuching area of Sarawak (1?29'N, 1 10?10'E), the site of our observations. Daily maxima and minima average 310 and 22?C (Fogden 1972), and the annual variation in daily mean temperature is only about 2?C (Briinig 1969, 1971). The relative humidity seldom drops below 60 percent and is usually close to 100 percent in the forests (Fogden 1972). Day length varies by only 10 minutes throughout the year. Annual rainfall at Kuching is about 4000 mm, and all months have rain (Walter and Lieth 1967, Briinig 1969, Fogden 1972). The area has Sarawak's most variable rainfall and thirty-day periods of relative drought (with less than 100 mm) can occur from March until September (Briunig 1969, 1971). The heaviest rainfall is brought by the northeast monsoon from December through February (Fig. 1A), when all-day rains can occur; at other seasons rain is mostly from convectional afternoon I Received 27 March, revision accepted 26 September 1984. BIOTROPICA 18(1): 51-55 1986 51 This content downloaded from 207.46.13.120 on Wed, 14 Sep 2016 05:47:06 UTC All use subject to http://about.jstor.org/terms

Heath Forest on Borneo is a forest type mostly found between the transitions from the peat-swamp forests in lowlands to the Dipterocarp Forest in hillier areas. Heath forest soil structure is characterized by a dominant sand layer with a thin organic horizon on top. Tropical Heath Forest has been understudied and undervalued for many years, considered as a low-diversity habitat due to a nutrient-poor sandy soil, unable to aggregate and bind nutrients, resulting in stunted, low canopy forest. Despite its reputation, our research in the KHDTK Mungku Baru(it is a Forest Area with Special Purpose (KHDTK)) in southern Central Kalimantan is revealing heath forest of remarkably high quality, with large trees, high canopy and high biodiversity, including important endemic and emblematic flora and fauna species. Fourteen 30 m x 30 m nested plots were established, where all the trees ≥ 10 cm diameter breast height (DBH) were identified and measured. Additional 5 x 5m and 2 x2 m nested plots were used to define the micro-habitat and soil composition, determining the pH, organic layer depth, water moisture, and canopy cover. A total of 1,007 trees were recorded, representing 87 species in 58 genus and 40 families. Soil layers exhibited visual differences and analysis of soil composition was used to define 2 sub-habitat types of Heath Forest, named as Black sand Heath Forest (BHF) and White sand heath forest (WHF). Significant differences were found on peat/organic layer depth (BHF 26.4 cm; WHF 6.1 cm) and soil moisture (BHF 18.3 %; WHF 11.1 %). Independent analysis for the tree community compositions was done for each sub-habitat type. Few differences were found between sub-habitat types on DBH (BHF 18.9 ± 11.7 cm; WHF 18.6 ± 9.7 cm) and tree height (BHF 18.9 ±5.5 m; WHF 17.9 ± 5.4 m). Tree species composition analysis reveals in both cases a high species richness, with no differences in distribution (Simpson’s Diversity Index BHF=0.96; WHF=0.95) but significant differences in species abundance (Fisher’s alpha index BHF=23.74; WHF=18.01). BHF is a more homogeneous sub-habitat type, dominated by species belonging to Dipterocarpaceae (19.5 %), Myrtaceae (19.2 %) and Sapotaceae (13 %) families, whereas WHF is largely dominated by Dipterocarpaceae species (43.4 %) including Dipterocarpus borneensis and Shorea teysmanniana. The preliminary results of this study indicate that the Central Kalimantan’s Heath Forest presents high tree species diversity with high conservation value, with potentially 2 different sub-habitat types characterized by their soil and tree composition. This highlights the importance of protecting this rare and understudied habitat in the context of Borneo biodiversity conservation.

The study of nutrient use efficiency in a heath and a peat swamp forest was carried out in Palangkaraya, Central Kalimantan. There was a stronger correlation in the heath forest between nitrogen and phosphorus in above ground litterfall than in the peat swamp forest, and higher positive correlation between litterfall mass and nitrogen return via litterfall in the heath than in the peat swamp forest, compared to phosphorus. The heath forest used nutrient more efficiently than the peat swamp forest and thus was more efficient in retranslocating nutrients. This phenomenon is important for plants to adapt to the heath forest conditions. Both the heath and peat swamp forests in this study were more efficient in their nutrient use than the mixed dipterocarp forests. There was a specific pattern of NUEP (phosphorus used efficiency): the NUEP was higher when P in litterfall was low, suggesting a seasonal effect. Thus in the heath and peat swamp forests, plants use interesting and important nutrient use strategy to adapt to seasonal change.

Effects of El Niño drought on tree mortality and growth across forest types at different elevations in Borneo

Summary Tropical heath forests have accumulations of slowly decomposing organic matter at the soil surface. To test the hypothesis that ectomycorrhizas are more abundant than arbuscular mycorrhizas under such conditions, we compared the abundance of ectomycorrhizal (EcM) tree species, and the relative proportions of EcM and arbuscular mycorrhizal (AM) roots, in heath forest and lowland rain forest. The mycorrhizal status of trees in two heath forest and two lowland (mixed dipterocarp) forest plots in Brunei Darussalam was determined by literature and field survey. Fine‐root density, proportion of EcM roots, and fractional colonization of EcM and AM roots were measured in monoliths from organic and mineral soil. There was no difference in the relative basal area abundance (10–41%) of EcM trees, the proportion of EcM roots in monoliths (8–46%), or fractional colonization (90%) of EcM roots, between the two forest types. However, fractional colonization of AM roots was higher (54%) in heath forest than in mixed dipterocarp forest (27%). Our data do not support the hypotheses that ectomycorrhizas are more abundant in, or determine the floristic composition of, tropical heath forests.

Since the 1970s Southeast Asian peat swamp forests have been increasingly threatened by anthropogenic disturbance. Peat swamps act as refuge for many endangered species, and they may turn into a net producer of CO2 and greatly contribute to climate change if cleared and drained. As one of the main invertebrate decomposers in the tropics, termites are likely to play a major role in peat forests. In this paper, we used a grid-based sampling plot protocol to sample termites in Brunei. We sampled termite communities in pristine and selectively logged peat swamp forests, that we compared with termite communities sampled in heath and dipterocarp forests. More precisely, we determined: (i) termite species diversity in peat swamp forests, and (ii) how termites respond to peat swamp logging. We found that species richness was the highest in the mixed dipterocarp forest. Selective logging had limited impact on species richness in peat swamp forest, suggesting that termite communities are resilient to limited amount of perturbations. Further data are needed to better understand the impact peat swamp clearance has on termite populations and their contribution to climate change.

Canopy-top leaves of the dominant tree species from two 0.96-ha plots in Brunei, northern Borneo, were sampled for structural and chemical analysis. Thirteen species from the mixed dipterocarp forest at Andulau and 14 from the lowland heath forest at Badas were studied. The heath-forest species had significantly thicker leaves and were lower in nitrogen and ash concentration than those from the mixed dipterocarp forest. There were no significant differences between the two species groups in leaf mass per unit area (LMA), leaf fracture toughness, carbon concentration, δ13C, neutral detergent fiber concentration, sclerophylly index, and stomatal density. A significant negative correlation between %C and δ13C was found for the species from the mixed dipterocarp forest, but not those from the heath forest. The degree of sclerophylly measured in physical terms overlapped between the two sites to a considerable degree; however, all six species tested that were present in both plots had higher leaf fracture toughness in the heath forest. The possible reasons for the marked sclerophylly in the mixed dipterocarp forest are discussed.

InvasiveAcaciaspecies are known to modify soil properties, although effects are often site-specific. We examined the impact ofAcaciaspecies on the soils of intact and invaded habitats of two contrasting tropical lowland rain forest types in Brunei Darussalam: heath forest (HF) and mixed dipterocarp forest (MDF). Impacts on soil properties differed between the two forest types. Overall,Acacia-invaded HF soil recorded significantly higher gravimetric water content, pH and total P, K and Ca compared to the intact HF soil. In contrast, invaded MDF soil exhibited significantly higher organic matter content and total soil N, P, K and Mg compared to its intact habitat.Acacia-invaded MDF soils were more nutrient-enriched thanAcacia-invaded HF soils by the addition of threefold, threefold and fourfold total soil P, K and Mg, respectively. The positive effect of addition of total soil Ca was, however, fourfold greater in HF soil than MDF soil, indicating that the magnitude of impact on soil properties was strongly site-specific. Overall,Acaciainvasion significantly impacted soil properties in nutrient-rich MDF more than those of nutrient-poor HFs, indicating a potential vulnerability of MDFs to invasion.

Lowland forests in Central Kalimantan, Indonesian Borneo, are endangered by land conversion and the increasing frequency of severe drought. Knowledge of the tolerance of tropical trees to drought is urgent for the management of these lowland habitats. The short-term effects of drought on tree demography (mortality and growth) were investigated in an ever-wet riparian peat-swamp forest and a heath forest on coarse sandy soil after the 1997 El Nino Southern Oscillation (ENSO) event. This drought was unusually severe because little rain fell during the following rainy season. However, forest-wide mortality following the drought (1997–1999) was not critically high in the peat-swamp (6.13% yr−1) or heath (4.26% yr−1) forest. In both forests, standing trees frequently died during the dry season following the drought. The riparian peat-swamp forest was not flooded until 1998, after the prolonged drought in 1997. The hummock–hollow microtopography resulted in differential mortality of peat-swamp trees. On tall hummocks, standing death increased two-fold (4.99% yr−1) during the dry season, whereas uprooting decreased by one-third (0.85% yr−1) during the following rainy season. In contrast, tree growth was not affected by hummock height. Common canopy species were concentrated on tall hummocks and died standing more often than did understory species found in hollows, indicating species-specific mortality after the drought. The large stand basal area relative to the forest-wide growth rate in diameter suggested less resilience to drought by peat-swamp (45.6 m2 ha−1 and 0.0186 ln[cm] yr−1) than heath (27.9 m2 ha−1 and 0.0232 ln[cm] yr−1) forest. A single severe drought did not cause dramatic changes in the peat-swamp and heath forests; however, an increasing frequency of droughts similar in severity to that of the 1997 ENSO event may have the potential to alter the community structure and dynamics, leading to a consistent decline in Bornean lowland forests.

Allometric relationships between tree dimensions, aboveground forest structure and productivity were examined in tropical heath (kerangas) forest and peatland forest in Central Kalimantan, to determine the stand level properties of these forest types growing under stressful conditions, by comparing with those in mixed dipterocarp forests. In the peatland forest, tree density, trunk diameter-height relationships and aboveground biomass differed between sites, partly due to differences in disturbance history such as the intensity of selective logging in the past. The heath and peatland forests shared common characteristics such as high leaf mass per area and long leaf residence time at the stand level. Both forest types had high wood mass increment rates (maximum of 8.2 Mg ha−1 year−1 in the heath forest and 10.9 Mg ha−1 year−1 in the peatland forest), which fluctuated greatly during and after the severe 1997–1998 drought. The results here suggest that the heath and peatland forests maintain moderately high productivity under stressful conditions, probably owing to the adaptive leaf properties. The results also suggest that the aboveground forest structure of these forest types as well as peat deposit has the potential to play a significant role in the carbon balance in an area. To be able to properly conserve these forest ecosystems, more attention must be paid to elucidating the mechanisms maintaining primary productivity of heath and peatland forests.

Lowland cloud forests are well known from temperate regions, e.g. the coasts of California and northern Chile (Bruijnzeel 2001), but in the Tropics have remained uninvestigated. We tested the hypothesis that tropical lowland cloud forest (LCF) and lowland rain forest (LRF) exist as distinct forest types with a higher abundance of epiphytes in LCF and differing in epiphyte species composition and microclimate. Furthermore, these forest types seem to occur in close proximity to one another, with LCF in valleys and LRF on adjacent slopes. To validate this hypothesis, we compared epiphyte diversity and abundance at two localities in Central French Guiana (Saül, Nouragues Nature Reserve). Using the single rope technique (ter Steege & Cornelissen 1988), we climbed 48 canopy trees from putative LCF and LRF during a 6 month field trip to French Guiana. On each of the 48 target trees, we removed epiphytes growing in 24 sample plots of 600 cm². The plots were positioned at each cardinal direction in six height zones (Johansson 1974, Cornelissen & ter Steege 1989): trunk base, lower trunk, upper trunk, lower canopy, middle canopy, and outer canopy. Biomass of epiphytic angiosperms, pteridophytes, lichens and bryophytes was determined and three groups of epiphytic plants identified at species level: macrolichens, filmy ferns and liverworts. Trees were classified as belonging either to LCF or LRF based on geography and validated by microclimate measurements. Species were identified using appropriate methods for the different taxa, and overall forest species composition evaluated for each forest type and statistically compared. In total we found 39 (morpho-) species of macrolichens, 9 species of Hymenophyllaceae, and 129 liverwort species. LCF contained a significantly higher mean species number per tree for both liverworts (LCF: 33.6; LRF: 25.0) and Hymenophyllaceae (LCF: 2.4; LRF: 0.3) than LRF. Moreover, 8 species of Hymenophyllaceae and 21 of liverworts were statistically determined as indicator species for LCF. These indicators of LCF included shade epiphytes and generalists that also occur in montane forests. As LCF is more humid than LRF, the differences in liverwort and filmy fern diversity can be attributed to the greater atmospheric water content. Although the number of macrolichen species per tree was similar in both forest types, lichens with cyanobacterial photobionts (cyanolichens) were 2.5 times more common in LCF. Cyanolichens are known to prefer humid habitats and this study showed that they are good indicators for LCF. The observed differences in species diversity of liverworts, filmy ferns and cyanolichens support the hypothesis that LCF and LRF contain distinguishable epiphytic biodiversity, a finding which is further supported by the measurement of higher overall epiphyte biomass in LCF and more tree surface area covered by epiphytes (70 % in LCF, 15 % in LRF). Species composition differed greatly in all height zones for all studied groups of epiphytes. Hygrophilous taxa (shade epiphytes) were more common in LCF, while LRF harbored more xeric taxa (outer canopy specialists). Moreover, comparison of the vertical distribution of epiphyte species in LRF and LCF showed an upward shift of certain species of lichens, bryophytes and ferns inhabiting lower strata in LRF towards higher strata in LCF. It had been previously observed that morning fog was present in LCF of Saül (Montfoort & Ek 1990). Fog can lead to higher humidity by providing a surplus of liquid water. To investigate whether there was an increased incidence of fog in LCF over LRF, we measured air humidity, calculated vapor pressure deficit, and frequency and duration of fog. LCF plots were more humid than LRF plots during both wet and dry season. LCF experienced higher overall mean air humidity, while high humidity events occurred both more frequently and longer than in LRF. The overall higher humidity is caused by fog formation in LCF at night; at early morning the moist air lifts into the canopy and acts as a radiation shield. Vapor pressure deficit in LCF was calculated to be lower than in LRF, especially in the early morning and significantly longer in duration. The prolonged availability of high air humidity in LCF and the additional input of liquid water through fog enhance epiphyte growth and influence species composition and diversity in LCF by shortening the desiccation period and lengthening the period of photosynthetic activity of the plants.

Abstract. Samples of Microlepidoptera (including Pyraloidea) collected at light in mangrove forest, lowland mixed dipterocarp forest, and montane oak‐laurel forest in Borneo are compared. Diversity (Williams' alpha) is very high in lowland forest, with a value of 414; it is lower, 226, in montane forest and very much lower, 47, at the edge of mangrove forest. There is some evidence that apparent diversity increases with accumulation of samples. Samples from the three forest types have very few species in common and come from separate assemblages. Pyraloidea in samples taken 1km apart in lowland forest represent an assemblage common to the two sites but Microlepidoptera samples appear to represent slightly different assemblages. There are no abundant species in lowland or montane forest: species with more than ten individuals comprised less than 4% of the samples. Four common species in mangrove forest accounted for 34% of the sample. The proportion of Tineoidea, Gelechioidea and Pyraloidea is lower in montane forest than in lowland forest, while that of Yponomeutoidea and Tortricoidea is higher. Just eight families of Microlepidoptera account for 90% of the species in samples from all three forest types. The number of species of moths in Borneo is suggested to be in excess of 8500.