Short Com 805 Azimah Haji (Assessment).cdr ASSESSMENT OF SEEDLING ABUNDANCE, SURVIVAL AND GROWTH OF TWO DIPTEROCARP SPECIES IN PEAT SWAMP FORESTS OF BRUNEI DARUSSALAM HAZIMAH HAJI MOHD DIN, NOR BASIRAH BAKIRI, RAHAYU SUKMARIA SUKRI and FAIZAH METALI* Environmental and Life Sciences Programme, Faculty of Science, Universiti Brunei Darussalam, Gadong BE1410, Brunei Darussalam Received 31 January 2017 / Accepted 21 March 2018 ABSTRACT Dryobalanops rappa Becc. and Shorea albida Sym. are Bornean endemics of high conservation value and increasingly threatened by anthropogenic disturbances. In-situ study of seedling abundance and growth performance of these Dipterocarp species was conducted in two selected peat swamp forests of Brunei Darussalam, following a mast fruiting event in March–May 2014. Within six 6 x 6 m plots at each forest site, D. rappa seedlings at the Anduki peat swamp forest and S. albida seedlings at the Badas peat swamp forest were measured for abundance at the initial census in September 2014, as well as survival and relative growth rates (RGR) after a period of 5 months, with the final census in February 2015. We found significantly higher seedling abundance for D. rappa (1885 ± 208) than S. albida (160 ± 71). Significantly higher percentage survival was recorded for D. rappa seedlings (90.8 ± 2.2%) in comparison to S. albida -1 -1 seedlings (81.7 ± 2.2%). S. albida seedlings (0.24 ± 0.02 mm mm month ) showed significantly greater RGR in stem -1 -1 diameter than D. rappa seedlings (0.18 ± 0.02 mm mm month ), however, there were no significant differences in the RGRs based on seedling height, leaf number and biomass between D. rappa and S. albida seedlings. In terms of seedling abundance and percentage survival, D. rappa seedlings appeared to be more successful in regeneration and may potentially be used for rehabilitation of degraded tropical peat swamps and other forest types. Our results suggested that greater conservation efforts of peat swamps must be made to protect the Bornean endemic plant species, in particular S. albida. Keywords: Borneo, Dipterocarpaceae, Dryobalanops rappa, relative growth rates, Shorea albida INTRODUCTION Peat swamp forest is a unique ecosystem that represents the second major forest type in Brunei Darussalam, accounting for 15.6% (or 90,884 ha) of Brunei's forest (Wong et al. 2015; Forestry Department 2016). It is mainly located in the Belait district, interconnecting with the peat swamps of the Baram basin in Sarawak. Bornean peat swamp forests are ombrogenous and have six 'phasic communities', each consisting of distinct plant communities (Anderson 1963). Over the years, there has been a significant reduction in peat swamps in Brunei Darussalam mainly due to infrastructure development and forest fires (Pg Harun 2015; Wong 2016). Peat swamps house unique flora, some of which are endemic and increasingly threatened in their natural ranges due to anthropogenic disturbances such as legal or illegal logging, forest fires and land-use changes (Yule 2010; Posa et al. 2011). Most tree families in lowland dipterocarps are found in peat swamps, but many peat swamp species are restricted and physiologically adapted to this extreme forest environment (Ng & Ibrahim 2001). In Brunei Darussalam, extensive stands of Dryobalanops rappa Becc. or 'Kapur paya' exist on shallow peat overlying sand in Lumut and Anduki, while pure stands of Shorea albida Sym. occur in the 'padang alan' and 'alan bunga' peat swamp forests of Badas, both in the Belait District (Anderson 1964; Ashton et al. 2003; Wong et al. 2015). The Anduki peat swamp forests experienced massive forest fires during the * Corresponding author: faizah.metali@ubd.edu.bn BIOTROPIA 5 2 8 148 154 Vol. 2 No. , 201 : - DOI: 10.11598/btb.2018.25.2.805 148 1997–1998 El Niño drought (Wooster et al. 2012), resulting in fragmented stands of intact D. rappa existing within an otherwise developed area. Low regeneration rates have been observed in natural D. rappa populations (Wong & Kamariah 1999), and this species is increasingly threatened from illegal logging (Phillips 1998). The Badas peat swamps consist of gregarious stands of S. albida that are decreasing in population density and have been showing few signs of natural regeneration for the past 30 years (Kobayashi 1998). The IUCN Red List classifies S. albida as endangered due to rapid population loss within its natural forest ranges, coupled with a regeneration status that is reported to be virtually non-existent (Ashton 1998). Furthermore, S. albida is endemic to north and west Borneo (Ashton 1998) and so the remaining stands in the Badas peat swamps in Brunei are likely to be one of the few remaining intact stands of S. albida in Borneo and globally (Forestry Department 2014). Both D. rappa and S. albida are important timber tree species that rely on irregular mass flowering and mast fruiting episodes as a means of their natural regeneration (Appanah & Turnbull 1998). Although several studies have been conducted on the survival and growth of Dipterocarpaceae seedlings in Bornean forests (Turner 1990; Delissio et al. 2002; Nakagawa et al. 2005; Shimamura et al. 2006; Takeuchi & Nakashizuka 2007; Daisuke et al. 2013), only a few have focussed specifically on peat swamp species (Ibrahim 1996; Gavin & Peart 1997; Saito et al. 2005; Jans et al. 2012), and no study has been conducted on S. albida seedlings to date. Following a small mass flowering and a mast fruiting event in the Badas and Anduki peat swamps in March–May 2014, the abundance, survival and growth of D. rappa and S. albida seedlings at the understorey of these two peat swamp forests were assessed in Br unei Darussalam. Our study provides preliminary findings on two native Dipterocarp species that can potentially be utilised in efforts to naturally regenerate and rehabilitate disturbed peat swamp forests. MATERIALS AND METHODS The study was conducted in the Anduki and Badas peat swamps located in the Belait district, Brunei Darussalam, north-west Borneo, at distances of ca. 14 km from each other by road. A dominant dipterocarp species (Dipterocarpaceae) in each peat swamp site was selected. The Anduki peat swamp (4°37'39.00"N, 114°22'1.14"E) is located in the coastal areas of Belait district within the Anduki Forest Reserve and is dominated by Dryobalanops rappa Becc. The Badas peat swamp (4°34'9.12"N, 114°24'40.08"E) is located further inland, south of Seria and is mainly populated by Shorea albida Sym. A total of six plots (6 m x 6 m or 2 36 m each) plots were set up: three plots of Shorea albida at Badas and three plots of Dryobalanops rappa at Anduki. Plots were located ca. 50 m away from each other and each plot was set up with a mother tree of the respective species located at the centre of the plot. Abundance of D. rappa seedlings in Anduki and S. albida seedlings in Badas were quantified per plot at the initial census in September 2014, ca. 3–5 months after the mass flowering and mast fruiting events. Within each plot, 40 seedlings of either D. rappa (at Anduki) or S. albida (at Badas) were randomly chosen and tagged in September 2014. The seedling censuses were conducted twice, in September 2014 and after 5 months, in February 2015. The tagged seedlings were measured for percentage survival, stem height (measured from the point of measurement painted white on soil surface to the top leaf bud), stem diameter and number of leaves (counted fully expanded leaves, excluding heavily eaten leaves i.e. approximately 70% of lamina eaten and dead leaves) at both censuses. A total of 10 seedlings of each species were randomly chosen from outside each of the three study plots per census and harvested to provide estimates of initial and final dry biomass. At both harvests, seedlings were washed with distilled water, oven-dried at 60 C for 48 h and weighed. o The relative growth rate (RGR) based on stem height (RGRH), stem diameter (RGRD), number of leaves (RGRL) and biomass (RGRB) per 149 Seedling abundance, survival and growth of two dipterocarp species – Mohd Din et al. recorded higher survival and RGR for D. rappa seedlings planted in lowland mixed dipterocarp forest (Sukri 2010) and degraded heath forest (W. H. Tuah, unpubl. data). Natural disturbance within the understorey may influence the survival of tree seedlings (Appanah & Turnbull 1998) and can be an explanation for the low percentage survival of S. albida. Yamada (1997) reported that Badas peat swamp has higher incidences of fallen trees and presence of buttress roots on its forest floor compared to Anduki peat swamp. During the rainy season between December 2014 – January 2015 in Badas, S. albida seedlings may not survive when hit by fallen trees and branches, thus decreasing its survival percentage. Through the mast fruiting period, the S. albida seeds may fall on the false forest floor in Badas, which is formed from litter accumulation on buttress roots. This may lead to S. albida seedlings mortality as the false floor may fall to the peat when disturbed. Seedling predation and microenvironment also influence seedling survival, and it has been recorded elsewhere in Borneo that late fruiting of Shorea species increased the possibility of seed losses to predation (Curran & Webb 2000). Anduki peat swamp has different physiological environment compared to Badas peat swamp forest in terms of its natural disturbance. Fragmentation of the Anduki forest due to rapid forest fires may cause its forest floor to develop shallow litter and peat overlying sandy soil (Yamada 1997). The Anduki Forest Reserve is dependent on waterlogged conditions to maintain the peat bog (Yussof 2015) and D. rappa seedlings are well-adapted to waterlogged peat (Yamada & Suzuki 2004). Survival and growth of S. albida seedlings have been found to be negatively affected by low light intensity (Kobayashi 1998), water shortage during dry spells (Kobayashi 1998) and excessive water during rainy period (Dixon et al. 2013), which may be factors that explain their low survival rates in Badas. D. rappa is a light-demanding species (Ashton et al. S. albida 2003), while seedlings have been recorded as shade-intolerant (Kobayashi 1998; pers. obs.). Regardless of the light environment, light-demanders tend to possess larger specific leaf area and higher photosynthetic capacity, which result in greater carbon gain, and potentially higher survival, compared to shade- tolerant species (Ghazoul & Sheil 2010). Light has seedling over the five-month census period were calculated following Hunt (1982): RGR = (log We 2 – log W ) / (t – t ), W and We 1 2 1 2 1 where are stem height, stem diameter, total number of leaves or biomass and . To compute RGRB, t – t is 5 months2 1 seedlings were paired by ranked values of seedling biomass at the initial and final harvests. B e t we e n - s p e c i e s d i f f e r e n c e s s e e d l i n g abundance, percentage seedling survival and RGR values were determined using t-tests in R 2.15.2 (R Core Team 2014). All data were first explored to confir m the nor mality of residuals and homogeneity of variances, and where necessary, data was log -transformed, with the exception of 10 percentage sur vival, which was arcsine- transformed. RESULTS AND DISCUSSION Using the initial census survey, D. rappa seedlings at the Anduki peat swamp forest showed 2 significantly higher mean abundance per 36 m plots compared to S. albida seedlings at the Badas peat swamp (D. rappa: 1885 ± 208 vs. S. albida: 160 ± 71, p< 0.01). This is a probable reflection of the higher density of adult D. rappa trees in Anduki, compared to the more sparsely populated adult S. albida trees in Badas (pers. obs.). Additionally, the higher D. rappa seedling abundance may be due to higher abundance of flowering mother trees, as almost all mature D. rappa trees flowered at Anduki whilst not all mature S. albida trees flowered at Badas during the same mass flowering event in 2014 (pers. obs.). Other studies have similarly documented a positive relationship between the number of mother trees and seedling density, with the highest seedling densities found in areas with high adult abundance (Itoh et al. 1997; Webb & Peart 1999; Backlund 2013). Mean percentage survival of tagged D. rappa seedlings over the period of 5 months was significantly greater than S. albida seedlings (90.8 ± 2.2% vs. 81.7 ± 2.2%, p< 0.05). All relative growth rates (RGRs) data of both species showed similar growth rates (Fig. 1) that there were no significant differences in all relative growth rates (RGR) except for RGR in stem diameter (RGRD), in which D. rappa seedlings had significantly lower RGRD than those of S. albida seedlings (0.18 ± 0.02 vs. 0.24 ± 0.02 mm mm month ; p< 0.01; -1 -1 Fig. 1B). Other studies in Brunei Darussalam have BIOTROPIA Vol. 25 No. 2, 2018 150 been recognised to significantly influence survival and growth of Dipterocarp seedlings (Scholes et al. 1996; Whitmore & Brown 1996). For example, D. rappa S. albidaand saplings were planted in the open in ongoing reforestation trial plots of degraded waterlogged heath forests ( Kerapah forests) in Brunei Darussalam, and have performed successfully in terms of its survival and growth rates over a period of more than a year (W. H. Tuah, unpubl. data). It was found that S. albida seedlings had significantly higher RGRD compared to D. rappa seedlings. This suggests that in the shaded understorey of peat swamp forests, S. albida seedlings allocated more resources to stem diameter growth than height growth. Tropical tree species that preferentially invest resources into stem diameter growth and wood density typically exhibit traits that defend against herbivory and pathogens, as well as for the Figure 1 Differences in relative growth rates (RGR) for seedlings in Anduki and seedlings in Dryobalanops rappa Shorea albida Badas: (A) RGRH (stem height; cm cm month ), (B) RGRD (stem diameter; mm mm month ), (C) RGRL -1 -1 -1 -1 (number of leaves; leaf number month ) and (D) RGRB (biomass; g g month ). RGR data were determined for -1 -1 -1 the 40 tagged and seedlings, except for RGRB which was determined for the 10 seedlings D. rappa S. albida harvested outside each plot at each census. The asterisk sign within each RGR denotes significant differences of means between species (marked with red dots) using t-tests (*, < 0.05; **, <0.01; ***, < 0.001). NS=Non-p p p significant. 151 Seedling abundance, survival and growth of two dipterocarp species – Mohd Din et al. development of their root system (Kitajima 1994), all of which decrease investment into height growth. The Badas peat swamp forest has a flat, densely crowded canopy (Yamada 1997), which restricts light entry to the understorey and may further inhibit height growth of S. albida seedlings. These shade-intolerant S. albida seedlings (Kobayashi 1998) require ample light to grow in height. Higher growth rates of S. albida in the open areas than in the closed canopy forest was recorded in the ongoing rehabilitation trial plots in the Kerapah forests of Brunei Darussalam (W. H. Tuah, unpubl. data). Both the Dryobalanops rappa peat swamp forest in Anduki as well as the Shorea albida peat swamp forest in Badas have been identified as critical habitats that are of high conservation value (Forestry Department 2014). Peat swamps are highly vulnerable to fires, particularly during the dry season and when the water table have been lowered (Yule 2010). Changes in drainage and hydrological conditions significantly increase repeated fire events (Posa et al. 2011). Repeated fires in Anduki and Badas, especially during drier periods and drought events, coupled with slow seedling growth rates, will undoubtedly result in further losses of both D. rappa and S. albida populations. In the case of S. albida, this loss will be further exacerbated by the low number of survived seedlings and mother trees flowering at the same time (pers. obs.). CONCLUSION This study recorded significant findings on Dryobalanops rappa seedlings in Anduki and Shorea albida seedlings in Badas. D. rappa seedlings were more abundant than S. albida seedlings, and also showed higher percentage seedling survival. S. albida seedlings, however, appeared to invest more in stem diameter growth, as their relative growth rate in terms of stem diameter was significantly higher compared to D. rappa seedlings. We suggest that D. rappa seedlings may be suitable as a species that can be used to rehabilitate degraded peat swamp forests, but detailed, longer term studies are needed to further support this conclusion. Finally, given that peat swamps forests are fast disappearing due to natural and anthropogenic disturbances, their protection and conservation efforts should be prioritised to protect the Bornean endemic plant species, in particular S. albida. 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