REINWARDTIA Vol. 21. No. 2. pp: 55‒62 DOI: 10.55981/reinwardtia.v21i2.4391 55 NUTRIENT CONCENTRATIONS IN THREE NEPENTHES SPECIES (NEPENTHACEAE) FROM NORTH SUMATRA Received August 15, 2022; accepted August 26, 2022 MUHAMMAD MANSUR Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia. Kampus UI Gedung E, Level 2, Jln. Lingkar Kampus Raya, Pondok Cina, Beji, Depok 16424, Indonesia. Research Center for Ecology and Ethnobiology, National Research and Innovation Agency (BRIN), Jln. Raya Jakarta- Bogor Km. 46, Cibinong, Bogor 16911, Indonesia. Email: mansurhalik@yahoo.com. https://orcid.org/0000-0003-0372-4699. ANDI SALAMAH Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia. Kampus UI Gedung E Level 2, Jln. Lingkar Kampus Raya, Pondok Cina, Beji, Depok 16424, Indonesia. Email: salamah@sci.ui.ac.id. https://orcid.org/0000-0002-4074-8342. EDI MIRMANTO Research Center for Ecology and Ethnobiology, National Research and Innovation Agency (BRIN), Jln. Raya Jakarta- Bogor Km. 46, Cibinong, Bogor 16911, Indonesia. Email: emirmanto@yahoo.com. https://orcid.org/0000-0001-7121-9980. FRANCIS Q. BREARLEY Department of Natural Science, Manchester Metropolitan University, Chester Street, Manchester, M1 5GD, UK. Email: f.q.brearley@mmu.ac.uk. https://orcid.org/0000-0001-5053-5693. ABSTRACT MANSUR, M., SALAMAH, A., MIRMANTO, E. & BREARLEY, F. Q. 2022. Nutrient concentrations in three Nepenthes species (Nepenthaceae) from North Sumatra. Reinwardtia 21(2): 55‒62. — Nepenthes is a genus of carnivorous plants that are unique ornamental plants, but their nutrient concentration relationships have not been studied much, especially in endemic species on the island of Sumatra. So far, the analysis of the nutrient concentration in Nepenthes is mostly limited to leaves. There are few reports of nutrient concentrations in the pitcher fluid and the soil around where it grows. Leaves, pitcher fluid, and soil around the growth sites of each species i.e., Nepenthes sumatrana, N. spectabilis, and N. tobaica, from North Sumatra province were collected for nutrient analyses (N, P, K, Ca, Mg, and Na). The results showed that the nutrient concentrations in the leaves and pitcher fluid in the three Nepenthes species were generally low with those in the leaves greater than in the pitcher fluid. The concentration of nutrients in the leaves of N. sumatrana (lowland species) was least (except for N and Na) when compared to N. specta- bilis and N. tobaica (highland species), likely reflecting the poorly fertile soil. In contrast, the nutrient concentration in the pitcher fluid of N. sumatrana was greater than N. spectabilis and N. tobaica. When compared across an exten- sive data set, we show that leaf N does not change with elevation, whereas P declines and the N:P ratio increases with elevation, suggesting that Nepenthes plants are obtaining sufficient N from prey at higher elevations. Key words: Nepenthes, North Sumatra, nutrient concentration. ABSTRAK MANSUR, M., SALAMAH, A., MIRMANTO, E. & BREARLEY, F. Q. 2022. Konsentrasi nutrien pada tiga jenis Nepenthes (Nepenthaceae) dari Sumatra Utara. Reinwardtia 21(2): 55‒62. — Nepenthes digolongkan ke dalam tumbuhan karnivora yang saat ini berfungsi sebagai tanaman hias unik, namun hubungan konsentrasi nutriennya belum banyak dipelajari khususnya pada jenis-jenis endemik pulau Sumatra. Sejauh ini, konsentrasi nutrien yang dianalisis baru terbatas pada daun, belum ada yang melaporkan konsentrasi nutrien yang ada di cairan kantong dan tanah tempat tumbuhnya. Sampel daun, cairan kantong, dan tanah di sekitar tempat tumbuh tiga jenis tanaman yaitu Nepenthes sumatrana, N. spectabilis, dan N. tobaica, dikoleksi dari provinsi Sumatra Utara untuk dipelajari kan- dungan unsur haranya. Hasil menunjukkan bahwa konsentrasi unsur hara pada daun dan cairan kantong pada ketiga jenis Nepenthes yang diteliti pada umumnya adalah rendah. Konsentrasi unsur hara pada daun N. sumatrana (jenis dataran rendah) adalah lebih rendah (kecuali unsur nitrogen dan natrium) jika dibandingkan dengan N. spectabilis dan N. tobaica (jenis dataran tinggi). Sebaliknya konsentrasi unsur hara pada cairan kantong N. sumatrana lebih tinggi dibandingkan dengan N. spectabilis dan N. tobaica. Untuk sampel daun, jika dibandingkan dengan seluruh kumpulan data yang luas, N daun tidak berubah dengan elevasi, sedangkan P menurun dan rasio N:P meningkat dengan elevasi, menunjukkan bahwa tumbuhan Nepenthes memperoleh N yang cukup dari mangsa di elevasi yang lebih tinggi. Kata kunci: Konsentr asi unsur har a, Nepenthes, Su matr a Utar a. https://dx.doi.org/10.55981/reinwardtia.v21i2.4391 https://orcid.org/0000-0003-0372-4699 https://orcid.org/0000-0002-4074-8342 https://orcid.org/0000-0001-7121-9980 https://orcid.org/0000-0001-5053-5693 REINWARDTIA 56 [VOL.21 INTRODUCTION Nepenthes (Nepenthaceae) is a genus of dioe- cious climbing plants with the unusual yet fasci- nating habit of being carnivorous; they also func- tion as a unique ornamental plant (Mansur, 2006). The Indonesian archipelago has the greatest num- ber of Nepenthes species with diversity concen- trated on the islands of Borneo (Kalimantan) and Sumatra. The Bukit Barisan Mountains, which stretch from South Sumatra to Aceh, are the largest contributor to the high biodiversity in Sumatra (Malik et al., 2020), including of Nepen- thes species (Lee et al., 2006). Until now, 22 spe- cies of Nepenthes have been reported from North Sumatra province with 16 of them endemic to Sumatra (Mansur et al., in press.). Nepenthes often grow in marginal soils that are poor in nutrients, especially nitrogen (Clarke, 1997; Clarke, 2001; Moran & Clarke, 2010). Nitrogen, phosphorus and potassium often (co-) limit the growth of carnivorous plants (Ellison, 2006). For example, Brearley & Mansur (2012) reported that the foliar nitrogen concentrations of N. ampullaria, N. gracilis, N. rafflesiana, and N. x hookeriana were low in peat swamp forest (Sebangau National Park, Central Kalimantan). Nepenthes species occupy a broad elevation range from sea level to over 3,000 m elevation (N. lamii in New Guinea is the species found at the highest elevation) and so we might expect changes in foliar nutrient concentrations along such a broad gradient as has been seen in other tropical plant taxa (Tanner et al., 1998; Bauters et al., 2017). In addition to macronutrient elements, Nepenthes plants are also able to absorb metallic elements such as lead, as found in N. macfarlanei which grows in the montane forests of the Genting Highlands in Malaysia (Brearley, 2021). The function of the pitchers of Nepenthes is to passively capture prey (Phillipps & Lamb, 1996), via nectar secreted by glands under the lid (Kurata & Kurata, 2009), through a slippery peristome (Bauer et al., 2009) and through the aroma released (Clarke & Lee, 2004). These can all attract the prey that falls into the pitcher fluid (Bonhomme et al., 2011) that may be highly viscoelastic (Gaume & Forterre, 2007). Once the prey is trapped, it will be broken down by the broad range of enzymes found in the pitcher fluid (Takeuchi et al., 2011; Rottloff et al., 2016), and the nutrients are absorbed through glands in the absorption zone in the pitcher walls (Clarke & Lee, 2004; Moran et al., 2010). The relationship between the nutrient concentrations in the genus of Nepenthes and its habitat has not been studied much, especially in species from Sumatra. The objective of this study was to determine nutrient concentrations in N. sumatrana (lowland species), N. spectabilis, and N. tobaica (both highland species) (Fig. 1) that are protected by Indonesia’s law (Permen LHK No. 20 of 2018). Based on the Red List issued by the IUCN, the conservation status of N. sumatrana is Critically Endangered (CR) and N. spectabilis is Vulnerable (VU), whereas N. tobaica is of Least Concern (LC). With this paper we hope to contri- bute to our understanding of nutrient relationships in Nepenthes and make a comparison between lowland and highland species using data from Su- matra as well as an extensive data comparison across the geographical range of Nepenthes spe- cies. MATERIALS AND METHODS Study site Sampling was carried out in November 2019 in Aek Nabobar Village, Sidikalang, Central Tapanuli Regency (N: 01'35'41; E: 098'53'43; altitude 75 m asl) for N. sumatrana and in Lae Pondom Protected Forest, Gunung Sibuatan, Karo Regency (N: 02'53'38; E: 098'29'27; altitude 1,750 m asl) for N. spectabilis and N. tobaica, both in North Sumatra Province. In Aek Nabobar village, N. sumatrana grows in the lowlands at an altitude between 20 to 75 m above sea level (asl) in open areas with shrubby habitats. In general, the habitat of N. sumatrana has high air temperature, soil pH, and light intensity, but low air humidity and soil moisture. On the other hand, the habitat of N. spectabilis and N. tobaica is in the Lae Pondom Protected Forest, Gunung Sibuatan, Karo Regency at an altitude of around 1,750 m asl that has lower air temperature, light intensity and soil pH, but higher air humidity and soil moisture. Nutrient analysis was carried out at the Research Center for Ecology and Ethnobiology, National Research and Innovation Agency (BRIN), Indonesia. Sampling design Following the approach of Brearley & Mansur (2012), Brearley (2021), and Mansur et al. (2021), three plant samples from each species of Nepenthes (N. sumatrana, N. spectabilis, and N. tobaica) were collected for their leaves, namely the second leaf from the tip of the stem (estimated to be six months old), pitcher fluid (10 to 40 ml depending on the pitcher sampled) and the soil (ca. 100 g from 10 to 20 cm depth) from the rooting zone where they grew. Morphological parameters of each plant sampled were also recorded (e.g. stem, leaf, and pitcher length and width) along with leaf chlorophyll concentration on the leaf sampled for nutrient concentrations using a Konica MANSUR et al.: Nutrient concentration of Nepenthes from North Sumatra 2022] 57 Fig. 1. A. Nepenthes sumatrana (Miq.) Beck ex Tamin & M.Hotta. B. Nepenthes spectabilis Danser. C. Nepenthes tobaica Danser; from North Sumatra Province, Indonesia. Photos by M. Mansur . Minolta SPAD-502 meter with the value used be- ing the mean of three measurements per leaf. Experimental procedures Leaf and soil samples were dried at 50 o C for 5 days, then ground. The nutrient concentrations of soil and leaf nitrogen (N) were analyzed using a Yanako JM1000CN macro corder with a JMA 1000 autosampler. For other nutrients, leaves and soil were digested in a mixture of acids (H2SO4, HClO4, and HNO3) for 24 hours at 170 o C, the con- centrations of potassium (K), calcium (Ca), mag- nesium (Mg), and sodium (Na) were analyzed using an atomic absorption spectrophotometer (Shimadzu AA-6200) while the concentration of phosphorus (P) used a spectrophotometer (Shimadzu UV Mini-1240) with the vanadomolyb- date colorimetric method. Pitcher liquid was fil- tered and analysed using atomic absorption spectrophotometry (as above) or with the Nessler and vanadomolybdate colorimetric methods for N and P, respectively. Data comparison across an extensive elevational dataset Data of the nutrient concentration of three species of Nepenthes were compared between leaves, pitcher fluid, and soils using one-way ANOVAs with post-hoc Duncan tests. Leaf nutrient concentration data were compiled from the literature (see Mansur et al., 2021), to which were added additional data on leaf N and P from other studies (Moran & Moran, 1998; Clarke et al., 2009; Moran et al., 2001, 2003; Graefe et al., 2011; Bazile et al., 2012). The elevation of each location was sourced from the appropriate paper, and linear regressions were calculated between elevation and the relevant leaf nutrient or the N:P ratio. RESULTS Morphology The morphology of the three species studied differed, N. sumatrana growing in the lowlands and open areas, had shorter stems, but greater stem diameter, pitcher size and tendril length than N. spectabilis and N. tobaica. The pitcher of N. sumatrana is trumpet-shaped, while those of N. spectabilis and N. tobaica are cylindrical (Fig. 1). The leaf chlorophyll concentration (SPAD meter readings) of N. sumatrana was greater than N. spectabilis, but lower than N. tobaica (Table 1). Soil nutrient concentrations Soil is not only a place for plants to grow but also a source of nutrients for the plants themselves (Turner, 2001). The concentration of nutrients contained in it determines its fertility and there- fore populations of plants. The concentrations of N, P, Ca, and Na in the soil in the habitat of N. sumatrana (lowland) were lower and significantly different (Table 2) when compared to those in the habitat of N. spectabilis and N. tobaica (highland); in contrast the concentrations of K and Mg in the N. sumatrana habitat were greater than of N. spectabilis and N. tobaica and statistically signifi- cantly different (Table 2). A B C REINWARDTIA 58 [VOL.21 Leaf nutrient concentrations Leaves, apart from being a place for photosyn- thesis to occur, are also a store of nutrients (Turner, 2001). Results showed that the leaves of N. sumatrana contained the greatest concentra- tion of N and significantly more than N. spectabi- lis, but not significantly different to N. tobaica (Table 2). On the other hand, the concentration of P in the leaves of N. sumatrana was lower and significantly less than N. spectabilis, but not sig- nificantly different from N. tobaica, while the concentration of K in the leaves of N. sumatrana was lower and different from N. spectabilis and N. tobaica (Table 2). Calcium and Mg in N. suma- trana leaves were lower and significantly different when compared to N. spectablis and N. tobaica, whereas on the other hand the concentration of Na in the leaves of N. sumatrana was greater than in the leaves of N. spectabilis, but not significant- ly different from N. tobaica (Table 2). Pitcher fluid concentrations The function of fluid in the pitcher of Nepen- thes is as a nutrient solvent (Moran & Moran, 1998; Clarke, 2001), which helps in the process of breaking down trapped insects (Clarke et al., 2009) and is carried out by enzymes secreted in the pitcher (Wang, 2009; Takeuchi et al., 2011), so that the presence of this fluid is very important for the fulfillment of Nepenthes plant nutrition. Nutrient concentrations were lower in the pitcher fluid compared to the leaves or soil (when all data were considered as percentages). Potassium was the most abundant nutrient in the pitcher fluid followed by Na and then Ca; other nutrients were at low concentrations. Concentrations of N, P, and K in the pitcher fluid of N. sumatrana were greater (although not always significantly) than in the pitcher fluid of N. spectabilis and N. tobaica. Like- wise, N. sumatrana contained concentrations of micronutrients Mg, Ca, and Na in the pitcher fluid that were greater than N. spectabilis and N. tobaica (Table 2). Foliar nutrients in an extensive elevational dataset Foliar N concentrations across our extensive elevational dataset were very variable (0.21 to 1.75 % N) but we found that there was no change in Nepenthes foliar N concentrations with elevation (r 2 = 0.04, p = 0.23). Phosphorus concentrations were less variable (0.06 to 0.26 % P) and showed a significant decline with elevation (r 2 = 0.17, p = 0.023); consequently there was an increase in the N:P ratio with elevation (r 2 = 0.23, p = 0.007) (Fig. 2). Parameter Nepenthes sumatrana spectabilis tobaica Stem Length (cm) 136 ± 41 215 ± 28 207 ± 23 Diameter (mm) 10.4 ± 1.2 5.3 ± 0.3 3.3 ± 0.3 Internode length (cm) 3.3 ± 0.8 5.3 ± 0.9 5.2 ± 1.0 Leaves Length (cm) 33.7 ± 2.1 21.4 ± 1.6 11.9 ± 0.2 Width (cm) 6.0 ± 0.7 4.0 ± 0.4 2.0 ± 0.1 Thickness (mm) 0.45 ± 0.01 0.60 ± 0.03 0.41 ± 0.00 Chlorophyll (SPAD meter units) 46.8 ± 2.1 37.6 ± 2.6 51.3 ± 3.5 Pitchers Length (cm) 18.0 ± 1.6 18.5 ± 1.9 10.3 ± 0.2 Bottom girth (cm) 12.5 ± 1.0 6.6 ± 0.8 8.6 ± 0.1 Top girth (cm) 15.9 ± 0.1 7.4 ± 0.8 6.6 ± 0.1 Tendril length (cm) 38.0 ± 8.2 23.1 ± 4.2 12.2 ± 0.2 Table 1. Morphology of three Nepenthes species as measured from three samples in their natural habitat in North Sumatra province, Indonesia. Values are mean ± standard error. MANSUR et al.: Nutrient concentration of Nepenthes from North Sumatra 2022] 59 DISCUSSION Nepenthes sumatrana grows in lowland areas (20 to 75 m asl) in open habitats with limestone soil and is often found overgrown with shrubs and ferns – at the study site, the vegetation and soil was quite degraded and prone to fire (Mansur et al., in press.). In contrast, N. spectabilis and N. tobaica grow in a different habitat in highland secondary forests (1,750 m asl) with a mineral soil type overlain by an organic humus layer and under large trees that provide shaded canopy cover. The two habitats have different microclimates and soil properties, in particular, the organic carbon content of the soils differed markedly and was around 25% in the highland forest but less than 0.5% in the lowland location (M.M., unpublished data). The concentration of soil nutrients in the N. spectabilis and N. tobaica habitat is generally greater than the soil where N. sumatrana grows (N, P, Na, and Ca), although the concentration of K and Mg in N. sumatrana habitat is greater than in the habitat of N. spectabilis and N. tobaica. How- ever, this broad pattern was not reflected in the foliar nutrient concentrations as, in general, it was found that the nutrient concentration in the leaves and pitcher fluid in N. sumatrana had a higher concentration than the other two species indicating that soil nutrients are not always good predictors of foliar nutrients and that neither of them may be related to pitcher fluid nutrient concentrations. However, a measure of available soil nutrients would be more appropriate in future studies rather than the total nutrient concentrations as measured here. Broadly, the foliar nutrient concentrations in all three species were typical for Nepenthes as they were found in the centre of a PCA diagram presented by Mansur et al. (2021). We know remarkably little about the determi- nants of pitcher fluid composition but this is im- Table 2. Concentrations of nutrients (% dry weight for leaves and soil, mg l -1 for pitcher fluid) in three species of Nepenthes at the study site, North Sumatra province, Indonesia. Values are mean ± standard error with letters indicating differences with a Duncan’s test. BDL = Below detection limits. Species Nutrient N P N:P K Ca Mg Na Leaves sumatrana 0.87 ± 0.10 (b) 0.10 ± 0.001 (a) 8.43 ± 1.12 (b) 1.67 ± 0.01 (a) 0.12 ± <0.01 (a) 0.07 ± <0.01 (a) 0.42 ± 0.01 (b) spectabilis 0.21 ± 0.06 (a) 0.11 ± 0.001 (b) 1.90 ± 0.54 (a) 1.75 ± 0.01 (b) 0.29 ± <0.01 (c) 0.11 ± <0.01 (c) 0.33 ± 0.01 (a) tobaica 0.58 ± 0.10 (ab) 0.11 ± 0.001 (ab) 5.37 ± 0.90 (ab) 1.77 ± 0.01 (b) 0.23 ± <0.01 (b) 0.11 ± <0.01 (b) 0.40 ± 0.01 (b) Fluid sumatrana 2.08 ± 0.13 (b) 8.30 ± 0.29 (b) 0.25 ± 0.01 (b) 1740 ± 49 (a) 396 ± 15 (b) 12.0 ± 1.18 (b) 1056 ± 42 (b) spectabilis 1.51 ± 0.14 (ab) 6.30 ± 0.29 (a) 0.24 ± 0.01 (b) 1640 ± 45 (a) 293 ± 14 (a) 5.5 ± 0.78 (a) 765 ± 42 (a) tobaica 1.13 ± 0.13 (a) 7.26 ± 0.34 (ab) 0.15 ± 0.01 (a) 1590 ± 30 (a) 304 ± 15 (a) 6.4 ± 1.15 (a) 873 ± 42 (a) Soil sumatrana BDL 0.019 ± 0.001 (a) NA 1.74 ± 0.01 (b) 1.02 ± <0.01 (a) 1.09 ± <0.01 (c) 0.47 ± 0.02 (a) spectabilis 1.17 ± 0.17 (b) 0.025 ± 0.001 (b) 46.9 ± 5.16 (a) 1.67 ± 0.01 (a) 1.30 ± 0.01 (b) 0.50 ± <0.01 (a) 0.63 ± 0.02 (b) tobaica 1.17 ± 0.17 (b) 0.024 ± 0.001 (b) 48.0 ± 5.36 (a) 1.68 ± 0.01 (a) 1.55 ± 0.01 (c) 0.76 ± <0.01 (b) 0.59 ± 0.02 (b) REINWARDTIA 60 [VOL.21 portant due to the role of the pitcher fluid in influ- encing the microbial composition therein (Gilbert et al., 2020) and its role in aiding in prey diges- tion through the production of a range of enzymes. Similar to other studies, K and Na were the domi- nant ions in the pitcher fluid (Buch et al., 2013; Mansur et al., 2021). Buch et al. (2013) found that N and P were at very low concentrations in the pitcher fluid they studied but these were under artificial experimental conditions so, in natural habitats, we would expect the pitcher fluid nutri- ent concentrations to be greater due to the addition of insect carcasses and other organic debris. The pitcher of Nepenthes has an important role in sup- plying nutrients that are not available in the soil and the greater concentrations of nutrients in the pitcher fluid of N. sumatrana may be because it has a larger pitcher size and is thus able to catch more insects than N. spectabilis and N. tobaica. This statement is also supported by the results of a study by Moran & Moran (1998) who reported that N. rafflesiana which lacks N (from prey sources) in its leaves can lead to decreased photo- synthetic activity and reduced number of pitchers of smaller sizes than control plants. It is not known if pitcher fluid has greater nutrient concentrations in species in more nutrient-rich habitats or if faster -growing species have lower nutrient concentra- tions due to more rapid uptake from the pitchers but this could be the focus of future research. Ad- ditionally, it would be informative to relate the pitcher and leaf nutrient concentrations to the com- position and biomass of insects and other organic material collected in pitchers over a given time frame. Across our extensive elevational dataset, we found that there was no change in foliar N with elevation – this suggests that Nepenthes species may obtain sufficient N from their prey with changing environmental conditions, or that there may be alterations to the stoichiometric ratio of their prey (i.e. changes in the N:P ratio) as elevation increases. As insects become less abundant at higher elevation, the importance of animal faeces may increase (Chin et al., 2010) or Nepenthes may be able to increase soil N uptake via roots or even through recently-described underground pitchers to trap soil animals (Dančák Fig. 2. Relationship between the concentration of foliar nitrogen (N), phosphorus (P), and the N:P ratio in a range of Nepenthes species across their geographical range. Each point represents the mean of each species sampled at each location. MANSUR et al.: Nutrient concentration of Nepenthes from North Sumatra 2022] 61 et al., 2022). In contrast, foliar P concentrations did decrease with elevation and the N:P ratio increased indicating increasing phosphorus limita- tion of Nepenthes pitcher plants with elevation. This might more reasonably be considered to be a reduction in N limitation as the N:P ratios were very low overall with a median of 8.1 across our dataset. Declining P with elevation could be due to the presence of ultramafic sites at higher elevations in the dataset although this is unlikely as we would also expect declining K and Ca and increasing Mg (Proctor, 2003) which we did not see – additional data on nutrient concentrations of Nepenthes growing in ultramafic substrates would also help test this further. CONCLUSION Nutrient concentrations in leaves and pitcher fluid in the three Nepenthes species studied (N. sumatrana, N. spectabilis, and N. tobaica) were generally low. The concentration of soil nutrients in the habitat of N. sumatrana in the lowland were generally lower than in the habitat of N. spectabilis and N. tobaica in the highland but nutrient concen- trations in the leaves and pitcher fluid of N. sumatrana (lowland species) were often greater than N. spectabilis and N. tobaica (highland spe- cies). Further consideration of environmental con- trols over foliar nutrient concentrations and their linkages with pitcher fluid nutrients and how this is important for nutrient uptake processes are strongly warranted in additional Nepenthes spe- cies. ACKNOWLEDGEMENTS This research was funded by a grant from The Mohamed bin Zayed (MbZ) Species Conservation Fund, Abu Dhabi, on 28 April 2019 with project number 192521032. Thanks to Nicolas Heard, the Head of Fund Management at MbZ Species Conservation, and Dr. Johanna Rode-Margono for help and support of this research. Special thanks to Heru Hartantri, Fauzi Rachmat, Yusran E. Ritonga and Mhd. Rafi’i M. 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