BIOTROPIA Vol. 30 No. 2, 2023: 220 - 231 DOI: 10.11598/btb.2023.30.2.1896 220 DIVERSITY, ECOLOGY AND CONSERVATION STATUS OF NEPENTHES IN WEST SUMATRA PROVINCE, INDONESIA MUHAMMAD MANSUR1,2*, ANDI SALAMAH3*, EDI MIRMANTO2 AND FRANCIS Q. BREARLEY4 1Postgraduate Biology Study Program, Faculty of Mathematics and Natural Sciences, Universitas Indonesia, Depok, West Java, 16404, Indonesia. 2Research Center for Ecology and Ethnobiology, Indonesian National Research and Innovation Agency (BRIN), Jalan Raya Jakarta-Bogor, Km 46, Cibinong Science Center, Cibinong, West Java, 16911, Indonesia. 3Cellular and Molecular Mechanisms in Biological System (CEMBIOS) Research Group, Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Indonesia, Depok, West Java, 16404, Indonesia. 4Department of Natural Science, Manchester Metropolitan University, Chester Street, ,,,,jManchester, M1 5GD, UK Received 14 February 2023 / Revised 11 April 2023 /Accepted 12 April 2023 ABSTRACT Nepenthes is the largest carnivorous plant genus present in Indonesia. There are 39 species of Nepenthes pitcher plants recorded in Sumatra from lowland to montane forests, and 34 of them are endemic; this represents the greatest species diversity of Nepenthes after Borneo. Field studies were conducted in 2021 and 2022 to increase our knowledge of the diversity, habitats and distributions of Nepenthes in West Sumatra province. Twenty-three species of Nepenthes were recorded from the province, consisting of 15 highland species, 4 mid-elevation species and 4 lowland species. Ecophysiological studies conducted at Bukit Malalak showed clumped distributions of N. bongso, N. dubia, N. eustachya and N. rhombicaulis. Foliar and pitcher fluid nutrient concentrations were found to be similar to those cited in other recent studies although growth rates were slightly more rapid than at Gunung Talang. Bukit Malalak is a new locality for two threatened species, namely N. dubia (CR) and N. rhombicaulis (VU), enlarging their extents of occurrence. In total, nine species from West Sumatra are threatened and conservation actions are urgently needed for these and other Nepenthes species remaining on the island. Keywords: associations, carnivorous plants, diversity, ecology, foliar nutrients, Indonesian Nepenthes, montane forest, Red List, West Sumatra INTRODUCTION Nepenthes is the only genus in the Nepenthaceae family (Phillipps & Lamb 1996; Clarke 2001). Nepenthes are climbing lianas that produce characteristic fluid-filled pitchers extending from tendrils at the end of leaf-like phyllodes. The pitchers have a range of adaptations to attract, catch, retain and digest mostly insect prey (Moran & Clarke 2010). The Indonesian archipelago, with a land area of 1,919,440 km2, is in the centre of the distribution of Nepenthes (which extends from Madagascar to New Caledonia). In 2021, 80 species, or approximately 44 % of all Nepenthes (181), were recorded from Indonesia (Mansur et al. 2021), with diversity concentrated in Borneo and Sumatra. Over the past few decades, many new species have been described, particularly in Indonesia, Malaysia and the Philippines. In the last three years alone, three new species have been described in Sumatra: N. putaiguneung Al Farishy, Metusala & Jebb in Kerinci Seblat National Park (Metusala et al. 2020), N. longiptera Victoriano in Aceh (Victoriano 2021) and N. harauensis Hernawati, R. Satria & Chi.C.Lee in West Sumatra (Hernawati et al. 2022b). There are now 39 Nepenthes species recorded in Sumatra (Hernawati et al. 2022a). Mansur et al. (2022a) recently documented the 22 species found in the province of North Sumatra, but information from other provinces remains poor. This is particularly true of the provinces through which the Barisan Mountains run, as these are likely to harbour the highest diversity of *Corresponding author, email: mansurhalik@yahoo.com/ salamah@sci.ui.ac.id mailto:mansurhalik@yahoo.com mailto:salamah@sci.ui.ac.id Diversity, Ecology and Conservation Status of Nepenthes in West Sumatra Province, Indonesia – Mansur et al. 221 Nepenthes due to their topographic variation (Nerz 2005). Furthermore, there are few ecophysiological studies of Nepenthes species endemic to Sumatra, in contrast to those in Borneo (but see Pavlovič et al. 2009, 2010; Moran et al. 2012; Mansur et al. 2022b). West Sumatra has a diverse topography, ranging from lowlands (< 500 m asl) to mountains (> 2000 m asl), with a broad range of associated microclimates and geologies. These conditions allow this province to support a high diversity of Nepenthes species. The estimated forest cover in West Sumatra is 1,897,911 ha, of which 41.7% is protected forest, 15.8% is production forest and 42.5% is within nature reserves and nature conservation areas (Dinas Kehutanan Sumatra Barat 2018). The aim of this study was therefore to determine the species diversity, distribution, population, habitat and ecology of Nepenthes in West Sumatra province. MATERIALS AND METHODS Field studies were conducted in October 2021 and October 2022 (totalling four weeks) in Agam Regency (Bukit Malalak and Gunung Singgalang), Limapuluh Kota Regency (Air Putih Nature Reserve, Batu Karang-Harau, Kelok Sembilan and Palupuah), Solok Regency (Gunung Talang) and around the city of Padang (Figure 1). Exploration was conducted to inventory the species of Nepenthes in each study location. Further study of literature, along with examination of herbarium specimens at Herbarium Bogoriense-Cibinong, took place in May and June 2022 to add information about the species of Nepenthes in West Sumatra; Pasaman Regency was only studied through a review of literature and herbarium specimens. We further focused on at Bukit Malalak (00°09 S; 100°23' E) where three plots of 0.09 ha each (10 m × 90 m) were established to determine the abundance of Nepenthes and the tree species growing in their habitat. Each species of Nepenthes in the nine subplots (10 × 10 m each) and their positions (x and y) were recorded. Trees (Ø ≥ 5 cm) in each subplot were identified and their trunk diameter, total height and positions (x and y) were measured. All data collected was processed and analysed according to the Mueller-Dombois & Ellenberg method (1974) to obtain values for basal area (BA), relative frequency (RF), relative density (RD), relative dominance (RDo), and importance value index (IVI). A few individuals of each Nepenthes species were numbered with small aluminium tags, and the top leaf of each individual was punched with a small hole using a paper hole-punch. After 12 months, the plants still living were re-censused and the stem length and number of leaves of each individual were re-recorded. Figure 1 Map of six study sites in four regencies/cities in West Sumatra province (study site 1: around Padang city (00°60' S; 100°23' E); study site 2: Gunung Talang (00°59' S; 100°41' E); study site 3: Gunung Singgalang (00°24' S; 100°20' E); study site 4: Bukit Malalak (00°09' S; 100°23' E); study site 5: Kelok Sembilan (S: 00°04' S ; 100°42' E), Air Putih Nature Reserve and Palupuah (00°03' S; 100°41' E); study site 6: Batu Karang-Harau (00°03' S; 100°44' E). BIOTROPIA Vol. 30 No. 2, 2023 222 Interspecific associations between plant species were calculated using a 2 × 2 contingency table (Ludwig & Reynolds 1988) on species that had an IVI > 10 % (Zulkarnaen et al. 2017). The calculated χ2 value was then compared with the χ2 table at the 5 % test level. If the value of χ2 was greater than that in the χ2 table at the 5 % test level, then there was an association between the two species, whereas if the value of χ2 was less than that in the χ2 table, then there was no association (Mueller- Dombois & Ellenberg 1974). The strength of the associations were then calculated using the Ochiai (1957) index with values ranging from 0 to 1, wherein the stronger the association between the two plant species, the closer the index value is to 1 (Ludwig & Reynolds 1988). Equations are presented in more detail in Mansur et al. (2022a). Finally, to determine the spatial distribution of each Nepenthes species (i.e. regular, random or clumped), Morisita’s (1959) index of dispersion was calculated using a quadrat size of 10 m × 10 m. Laboratory Procedures Analysis of nutrient concentrations was carried out on samples of N. bongso Korth., N. dubia Danser and N. rhombicaulis Sh.Kurata from Bukit Malalak. Leaf samples were dried in an oven at 60 °C for three days and then ground with a pestle and mortar. Two ml of mixed acid (sulphuric acid, nitric acid and perchloric acid) was added to 0.2 g of leaf material and heated on a hotplate at 170 °C until the solution was clear; samples were then diluted to a final volume of 10 ml before analysis. Phosphorus concentration was determined using a colorimetric method, in which 1 ml of sample was added to 3 ml of distilled water and then reacted with 1 ml of P dye; the yellow colour of the sample was measured using a Shimadzu BioSpec-Mini 1240 UV-vis spectrophotometer at 450 nm. Nitrogen concentration was also determined by a colorimetric method, where 2 ml of the sample reacted with 4 ml of sodium phenoxide and 4 ml of 5% NaOCl; the blue colour of the sample was measured using a spectrophotometer as above but at a wavelength of 636 nm. Other elements were determined with atomic absorption spectrophotometry using a Shimadzu AA-6800. Pitcher fluid was analysed as above after being filtered to remove any debris. RESULTS AND DISCUSSION Diversity In total, 23 species of Nepenthes were recorded from West Sumatra province, comprising 18 species documented during the field surveys, two species represented by herbarium specimens (N. jamban Chi C.Lee, Hernawati & Akhriadi: BO.1979938 and N. lingulata Chi C.Lee, Hernawati & Akhriadi: BO.1979937), two species documented from the region in literature records, i.e., N. izumiae Troy Davis, C.Clarke & Tamin (Clarke et al. 2003) and N. jacquelineae C.Clarke, Troy Davis & Tamin (Clarke 2001), and one species also indicated for the region via a credible second- hand source, namely N. naga Akhriadi, Hernawati, Primaldhi & M.Hambali (Putra-RSN Nepenthes Nursery, pers. comm.; Table 1). The majority of species documented are considered highland species (15), with four species each of mid-elevation and lowland species. Seven species are restricted to West Sumatra, 11 are found across other provinces of Sumatra (in addition to West Sumatra) and five are also found on other Indonesian islands. Nine species have been assessed as having a threatened status (2 × VU, 2 × EN, 5 × CR) against the International Union for Conservation of Nature (IUCN) 3.1 criteria (IUCN 2001) (Clarke et al. 2000a, b, c; Clarke 2014; Hernawati & Clarke 2014; Hernawati et al. 2014; Cross et al. 2020). Limapuluh Kota Regency had the greatest number of species (9), followed by Pasaman Regency (8 species), Solok and Agam Regencies (7 species each) and then Padang City, with just 2 species. We also found four natural hybrids: N. talangensis Nerz & Wistuba × N. bongso and N. talangensis × N. inermis Danser at Gunung Talang, and N. eustachya Miq. × N. albomarginata W.Lobb ex Lindl., and N. gracilis Korth. × N. eustachya in Air Putih Nature Reserve. Diversity, Ecology and Conservation Status of Nepenthes in West Sumatra Province, Indonesia – Mansur et al. 223 Table 1 Habitat, distribution, elevation and conservation status of the 23 Nepenthes species recorded from West Sumatra province. Species in bold were recorded from the field survey Nepenthes Habitat Regency Elevation Distribution IUCN Red List category AG LM PD PS SL adnata Tamin & M.Hotta ex Schlauer Forest ● M/H WS EN [D] albomarginata W.Lobb ex Lindl. Forest/Shrubland ● ● M/H Indo LC ampullaria Jack Shrubland ● L/M Indo LC bongso Korth. Forest ● ● H S LC dubia Danser Mossy forest ● H WS CR [B1+2e] eustachya Miq. Forest/Shrubland ● ● ● M S LC gracilis Korth. Shrubland ● ● ● L Indo LC harauensis Hernawati, R.Satria & Chi.C.Lee Forest ● H WS - inermis Danser Mossy forest ● H S LC izumiae Troy Davis, C.Clarke & Tamin Forest/Shrubland ● H WS LC jacquelineae C.Clarke, Troy Davis & Tamin Mossy forest ● H WS CR [B2ab(v) C2a(i)] jamban Chi C.Lee, Hernawati & Akhriadi: Mossy forest ● H S CR [B2ab(v) C2a(i)] lingulata Chi C.Lee, Hernawati & Akhriadi: Forest ● M S CR [B2ab(v)] longifolia Nerz & Wistuba Forest/Riparian ● M S LC mirabilis (Lour.) Druce Shrubland ● L Indo LC naga Akhriadi, Hernawati, Primaldhi & M.Hambali Forest ● H S VU [D2] pectinata Danser Forest ● ● ● H S LC reinwardtiana Miq. Shrubland ● ● L/M Indo LC rhombicaulis Sh.Kurata Forest ● H S VU [D2] singalana Becc. Forest ● H S LC spathulata Danser Forest/Mountain peak ● ● H S LC talangensis Nerz & Wistuba Forest/Mossy forest ● H WS EN [C2b] tenuis Nerz & Wistuba Forest ● H WS CR [A2] Notes: AG = Agam, LM = Limapuluh Kota, PD = Padang City, PS = Pasaman, SL= Solok; L = Lowland, M = Mid- elevation, H = Highland; WS = West Sumatra only, S = Sumatra only, Indo = other islands in Indonesia (in addition to Sumatra); LC = Least Concern, VU = Vulnerable, EN = Endangered, CR = Critically Endangered, - = not yet assessed against IUCN Red List criteria. In our survey, conducted across five regencies in West Sumatra, we recorded 23 species of Nepenthes, 18 of which are endemic to the island of Sumatra. This number is comparable to our survey in North Sumatra (22, including two taxa yet to be formally described; Mansur et al. 2022a), with 12 species common to both surveys. Nepenthes eustachya, N. gracilis and N. pectinata Danser are three species whose distribution is quite broad, as they are found in three regencies/cities; indeed, N. gracilis is widespread not only in western Indonesia, but also in Peninsular Malaysia and southern Indochina. Other species, however, are more limited, notably N. talangensis, which is found only on Gunung Talang (Solok Regency; Nerz & Wistuba 1997), N. jacquelineae in Pasaman Regency (Clarke 2001) and N. harauensis in Limapuluh Kota Regency (Hernawati et al. 2022b), all three of which are the type localities for those species, while N. jamban, N. lingulata and N. naga are found not only in Pasaman Regency (West Sumatra), but also in Mandailing Natal Regency (North Sumatra), on the border between West Sumatra and North Sumatra. Population Nepenthes population measurements were only carried out at Bukit Malalak. In the study plots, N. bongso generally grew as an epiphyte under a shady canopy with a small population (Plot 2), while in open areas (mountain peak), it grew terrestrially with a larger population (Plot 1). In a total plot area of 0.27 ha, seven individuals of N. BIOTROPIA Vol. 30 No. 2, 2023 224 dubia were found: four in Plot 1 and three outside of the plot in mossy forest (mountain peak), growing terrestrially under a slightly open canopy (Table 2). Nepenthes eustachya was abundant in Plot 3 and grew terrestrially in shady areas. Thirteen individuals of N. rhombicaulis were found in Plot 1 and ten were found in Plot 2, where they grew terrestrially in shady areas. Morisita’s index was greater than 1 for all species in all plots, indicating a clumped distribution; the exception was of N. rhombicaulis in Plot 2, which had a value of 0.80, indicating a more random distribution. These clumped distributions are in keeping with earlier studies (Adam 2002; Damit et al. 2017), which is likely due to similar habitat requirements for light or sufficiently moist soil, for example. More advanced statistical techniques, such as those based on Ripley’s K, are likely to be more informative regarding spatial patterns if sufficient individuals are measured (Brearley et al. 2023). Table 2 Number of individuals of four Nepenthes species in three plots each of 0.09 ha at Bukit Malalak, Agam Regency (Sumatra). Nepenthes Elevation (m) Plot 1 (1586 m asl) 2 (1329 m asl) 3 (1186 m asl) Total bongso 1300–1600 64 6 0 70 dubia 1550–1600 4 0 0 4 eustachya 1150–1300 0 0 50 50 rhombicaulis 1300–1600 13 10 0 23 Figure 2 Nepenthes distributions in three 0.09 ha plots on Bukit Malalak, Agam Regency (Sumatra). Open circles show locations of each tree species with larger circles indicating trees of larger stem diameter. Coloured circles indicate locations of Nepenthes individuals of different species Diversity, Ecology and Conservation Status of Nepenthes in West Sumatra Province, Indonesia – Mansur et al. 225 Habitat At the Bukit Malalak study site, Nepenthes plants grew in primary forest with very steep sloping. The forest’s condition was intact, with few signs of human disturbance. In the total plot area of 2700 m2, there were 416 individual trees (Ø ≥ 5 cm) recorded, comprising 34 species, 29 genera and 20 families. Myrtaceae was the most species-rich family, with eight species, five of which were Syzygium. The five dominant tree species in the Nepenthes habitat were Ternstroemia gymnanthera (Wight & Arn.) Bedd. (IVI = 42.1) followed by Syzygium zeylanicum (L.) DC. (28.5), Myrsine avenis (Blume) A.DC. (24.0), Rhodoleia championii Hook. (22.1) and Leptospermum javanicum Blume (19.1; Table 3). Table 3 List of tree species and their abundance in 0.27 ha of forest plots containing Nepenthes species at Bukit Malalak, Agam Regency (Sumatra) Species Family BA (m2) RD (%) RF (%) RDo (%) IVI (%) Ternstroemia gymnanthera (Wight & Arn.) Bedd. Pentaphylacaceae 1.330 22.1 6.04 14.0 42.1 Syzygium zeylanicum (L.) DC. Myrtaceae 1.100 11.5 5.37 11.6 28.5 Myrsine avenis (Blume) A.DC. Primulaceae 0.720 10.3 6.04 7.60 24.0 Rhodoleia championii Hook. Hamamelidaceae 0.860 7.69 5.37 9.02 22.1 Leptospermum javanicum Blume Myrtaceae 1.170 3.37 3.36 12.3 19.1 Syzygium sumatranum (Miq.) Widodo Myrtaceae 0.760 4.33 6.04 8.01 18.4 Castanopsis costata (Blume) A.DC. Fagaceae 0.500 4.33 6.04 5.26 15.6 Syzygium bankense (Hassk.) Merr. & L.M.Perry Myrtaceae 0.440 4.09 4.70 4.65 13.4 Gaultheria heterophylla var. latifolia (Blume) Kron & P.W.Fritsch Ericaceae 0.360 3.85 5.37 3.80 13.0 Pittosporum ferrugineum W.T.Aiton Pittosporaceae 0.350 2.16 5.37 3.71 11.2 Carallia eugenioidea King Rhizophoraceae 0.210 3.61 4.70 2.17 10.5 Eriosolena composita (L.f.) Tiegh. Thymelaeaceae 0.310 3.13 3.36 3.29 9.77 Neolitsea cinnamomea (Ridl.) Kosterm. Lauraceae 0.200 1.92 3.36 2.06 7.34 Tristaniopsis merguensis (Griff.) Peter G.Wilson & J.T.Waterh. Myrtaceae 0.200 1.92 2.68 2.11 6.72 Heptapleurum sp. Araliaceae 0.060 1.44 3.36 0.58 5.38 Dacrydium elatum (Roxb.) Wall. ex Hook. Podocarpaceae 0.160 0.96 2.68 1.68 5.32 Adinandra dumosa Jack Pentaphylacaceae 0.150 1.68 2.01 1.54 5.24 Pterophylla fraxinea D.Don Cunoniaceae 0.170 0.96 2.01 1.76 4.74 Syzygium acuminatissimum (Blume) DC. Myrtaceae 0.100 1.68 1.34 1.07 4.1 Calophyllum teysmannii Miq. Calophyllaceae 0.070 0.96 2.01 0.75 3.73 Polyosma ilicifolia Blume Escalloniaceae 0.050 1.20 2.01 0.49 3.71 Archidendron bubalinum (Jack) I.C.Nielsen Fabaceae 0.020 0.96 2.01 0.18 3.15 Symplocos adenophylla Wall. ex G.Don Symplocaceae 0.020 0.72 2.01 0.25 2.99 Schima wallichii (DC.) Korth. Theaceae 0.020 0.72 2.01 0.21 2.95 Elaeocarpus mastersii King Elaeocarpaceae 0.020 0.72 2.01 0.20 2.93 Litsea sp. Lauraceae 0.050 0.48 1.34 0.51 2.34 Wendlandia densiflora (Blume) DC. Rubiaceae 0.020 0.72 1.34 0.26 2.32 Lithocarpus conocarpus (Oudem.) Rehder Fagaceae 0.020 0.72 1.34 0.23 2.29 Myrica javanica Blume Myricaceae 0.040 0.48 1.34 0.39 2.21 Vaccinium lucidum (Blume) Miq. Ericaceae 0.010 0.24 0.67 0.09 1.00 Rhodamnia cinerea Jack Myrtaceae 0.010 0.24 0.67 0.07 0.98 Syzygium antisepticum (Blume) Merr. & L.M.Perry Myrtaceae 0.010 0.24 0.67 0.06 0.98 Garcinia lateriflora Blume Clusiaceae 0.004 0.24 0.67 0.04 0.95 Timonius flavescens (Jacq.) Baker Rubiaceae 0.003 0.24 0.67 0.03 0.94 Grand Total 9.517 Note: BA = basal area, RD = relative density, RF = relative frequency, RDo = relative dominance, IVI = importance value index BIOTROPIA Vol. 30 No. 2, 2023 226 Interspecific Associations The Ochiai Index showed that N. bongso was positively associated with N. dubia and strongly positively associated with Ternstroemia gymnanthera in Plot 1 (Table 4). In Plot 2, N. rhombicaulis was positively associated with N. bongso, but they were weakly associated in Plot 1. Nepenthes rhombicaulis was also strongly positively associated with five species with a very high Ochiai index in Plot 2 and, in Plot 3, N. eustachya had positive associations with seven species with a very high Ochiai index (Table 4). Adam (2002) also found positive associations between N. × kinabaluensis Sh.Kurata and N. villosa Hook.f. and Leptospermum recurvum Hook.f. (Myrtaceae) in montane forest in northern Borneo, so it would be valuable to determine the traits of the trees that Nepenthes tend to associate with. Furthermore, understanding which habitats and which particular tree species or communities certain Nepenthes species associate with may provide further insight into where these Nepenthes species may be found in other localities. Table 4 Chi-square (χ2) and Ochiai Index (OI) values showing inter-specific associations between Nepenthes bongso (Plot 1), N. rhombicaulis (Plot 2), and N. eustachya (Plot 3) and other Nepenthes species and the ten tree species with the greater IVIs at Bukit Malalak, Agam Regency (Sumatra) Species Plot 1: Association with N. bongso Plot 2: Association with N. rhombicaulis Plot 3: Association with N. eustachya Chi-squared (χ 2) Ochiai Index (OI) Chi-squared (χ 2) Ochiai Index (OI) Chi-squared (χ 2) Ochiai Index (OI) Nepenthes dubia + 0.61 (High) Absent Absent Absent Absent Nepenthes bongso NA NA + 0.74 (High) Absent Absent Nepenthes rhombicaulis - 0.25 (Low) NA NA Absent Absent Ternstroemia gymnanthera + 0.88 (Very high) + 0.88 (Very high) + 0.67 (High) Syzygium zeylanicum Absent Absent - 0.44 (Low) + 0.94 (Very high) Myrsine avenis + 0.50 (High) + 0.88 (Very high) + 0.88 (Very high) Rhodoleia championii - 0.25 (Low) + 0.77 (Very high) + 0.82 (Very high) Leptospermum javanicum + 0.53 (High) Absent Absent Absent Absent Syzygium sumatranum Absent Absent Absent Absent + 1.00 (Very high) Castanopsis costata Absent Absent + 0.80 (Very high) + 0.56 (High) Syzygium bankense Absent Absent - (Low) + 0.75 (Very high) Gaultheria heterophylla + 0.89 (Very high) + 0.66 (High) + 0.75 (Very high) Pittosporum ferrugineum Absent Absent - 0.00 (Very low) + 0.82 (Very high) Diversity, Ecology and Conservation Status of Nepenthes in West Sumatra Province, Indonesia – Mansur et al. 227 Growth Rates Leaf production rates and stem growth rates were quite variable within species. There were no significant differences in the rates among the four species measured over one year (only one individual of N. bongso could be measured, because the others died; Table 5). The mean stem growth rate was significantly greater on Bukit Malalak (42.1 ± s.e. 4.8 cm yr-1) than on Gunung Talang (29.9 ± 3.6 cm yr-1) (t = 2.06, p = 0.05), although the leaf production rate was not (9.8 ± 1.2 leaves yr-1 versus 7.3 ± 0.6 leaves yr-1, respectively; Mansur et al. in review); this could be due to the lower elevation of the plants studied on Bukit Malalak or simply the fact that different species were measured at each site (with the exception of N. bongso). It would be interesting to further examine the possible trade- offs between leaf and stem production rate and plant survival (Mansur & Brearley 2008), as has been done in tropical tree seedling studies (Brearly et al. 2016). Nutrient Concentrations Macronutrient concentrations in the leaves were greater than those in the Nepenthes pitcher fluid, and there were no significant differences in nitrogen or potassium concentrations between species, but phosphorus was greatest in the leaves of N. dubia and least in N. rhombicaulis. The concentrations of foliar magnesium were not significantly different between the three species; however, calcium was greatest in N. bongso and sodium was greatest in N. dubia and least in N. bongso. Pitcher fluid concentrations were variable, and there were few significant differences among species, although N dubia had notably lower P, K and Mg concentrations (Table 6). Our ecological studies on Bukit Malalak showed that the habitat of Nepenthes was an infertile Latosol (unpubl. data), indicated by the presence of a large number of Syzygium species and Tristaniopsis merguensis (Griff.) Peter G.Wilson & J.T.Waterh. This compares with more fertile volcanic Andosols as found on other mountains in the region, such as Gunung Singgalang and Gunung Talang. However, these differences were not reflected in the foliar N, P or K concentrations when compared with material from Gunung Talang (Mansur et al. in review), although N was greater and K was lower than the species from North Sumatra (Mansur et al. 2022b). In contrast, less Mg was noted in the leaves from Bukit Malalak than those from Gunung Talang (but more than those from North Sumatra) and less Ca but more Na was found in the Nepenthes leaves from Gunung Talang and North Sumatra. If the plants obtain sufficient nutrients from their insect prey, this may be one reason nutrient concentrations in the sampled leaves do not differ between locations despite contrasting soil fertilities. Indeed, we earlier showed that foliar N concentrations of Nepenthes did not vary along elevation gradients, although there was an impact on foliar P concentrations (Mansur et al. 2022b). Determinants of foliar nutrient concentrations will differ by species and locality. How they influence the performance of different Nepenthes species would be valuable further research. Table 5 Growth rates of four Nepenthes species in their natural habitat at Bukit Malalak, Agam Regency (Sumatra) over an twelve-month period (Oct 2021 to Oct 2022). Also shown are the environmental conditions and survival rates. Values are mean ± standard error Nepenthes Plot Conditions No. of individuals Survival (%) No. of new leaves produced Length of new stem produced (cm) bongso 2 Slightly shaded 1 33 5.0 24.6 dubia 1 Fairly open 3 100 9.7 ± 0.3 48.9 ± 7.8 eustachya 3 Shaded 3 100 13.3 ± 2.9 52.2 ± 8.0 rhombicaulis 2 Slightly shaded 4 100 8.5 ± 1.6 33.7 ± 7.6 BIOTROPIA Vol. 30 No. 2, 2023 228 Table 6. Nutrient concentrations in leaves and pitcher fluid of three Nepenthes in Bukit Malalak, Agam Regency (Sumatra). Values are mean ± standard error with letters indicating significant differences (at p < 0.05) with a Tukey’s test Element Leaves (%) Pitcher fluid (mg l-1) bongso dubia rhombicaulis bongso dubia rhombicaulis N 1.09 ± 0.02 a 1.01 ± 0.01 a 1.36 ± 0.22 a 0.97 ± 0.22 a 3.52 ± 1.44 a 1.09 ± 0.04 a P 0.10 ± <0.01 ab 0.14 ± 0.02 b 0.08 ± 0.01 a 5.04 ± 0.03 a 0.18 ± 0.05 a 4.51 ± 2.35 a K 1.32 ± 0.02 a 1.08 ± 0.18 a 1.10 ± 0.05 a 721 ± 363 a 6.72 ± 1.23 a 283 ± 163 a Ca 0.16 ± 0.02 b 0.05 ± 0.01 a 0.09 ± 0.02 a 491 ± 27 b 294 ± 4.6 ab 172 ± 86 a Mg 0.14 ± 0.01 a 0.12 ± 0.01 a 0.13 ± <0.01 a 92 ± 11 c 4.9 ± 0.2 a 50 ± 5.6 b Na 0.42 ± 0.04 a 0.92 ± 0.14 b 0.70 ± 0.02 ab 0.85 ± 0.03 a 1.48 ± 0.07 a 516 ± 296 a Conservation Status Of the 23 species reported from West Sumatra, nine have threatened conservation status, namely N. dubia (CR), N. jacquelineae (CR), N. jamban (CR), N. tenuis (CR), N. adnata Tamin & M.Hotta ex Schlauer (EN), N. talangensis (EN), N. tenuis Nerz & Wistuba (EN), N. naga (VU) and N. rhombicaulis (VU). At nearly 40 % of the known species in the province, this is a worryingly high proportion. Our research extends the ranges of N. jamban and N. lingulata from their type locality in North Sumatra (Lee et al. 2006) to West Sumatra based on herbarium collections deposited at Herbarium Bogoriense (BO) by Wewin Tjiasmanto and that of N. naga through personal communication (Putra). Previously, N. dubia was only known to grow on Gunung Talakmau, Pasaman and West Pasaman Regencies, at an elevation of 1800 to 2700 m asl (Clarke 2001), and Mandailing Natal Regency, North Sumatra (Sahal, pers. comm.). Our research also extends the known range of N. dubia to include Bukit Malalak, thereby increasing the size of the small, originally documented population and its extent of occurrence (EOO). This is positive, as species with larger ranges and population sizes are less prone to extinction; this species is currently listed as critically endangered, satisfying the Red List criteria B1+2e, i.e. it has a small geographic range and small population size (Clarke et al. 2000a; Cross et al. 2020). The EOO of N. rhombicaulis is also extended, having been formally documented only from Gunung Pangalubao near Lake Toba in North Sumatra, about 300 km distant. This species is currently assessed as Vulnerable under the Red List criterion D2, i.e. it has a restricted area of occupancy (Clarke et al. 2000b). Cross et al. (2020) listed N. tenuis as CR under criteria A2, i.e. a greater than 80% reduction in population over the last 10 years. They further considered that it might be extinct; however, we found this species growing in the Batu Karang-Harau area, albeit with a very small population of about 20 individuals. Despite extending the range and population of these species, they are still threatened, as we discuss below. The other six species are listed as threatened because of their restricted ranges and an observed decline in their population in the cases of N. jacquelineae, N. jamban and N. talangensis (Clarke et al. 2000c; Cross et al. 2020). Nepenthes harauensis has only recently been described (Hernawati et al. 2022b) and has not yet been formally assessed for the IUCN Red List; nevertheless, the restricted range of this species coupled with the rapid rate of environmental change in Sumatran ecosystems strongly suggests that it is likely to be threatened in its natural environment and would likely fall under the Endangered category if formally assessed (although we would need a better estimate of of its populations’ size and trajectory). Other species that might be found in West Sumatra province include N. putaiguneung, which was recently described from an unknown location in the extensive Kerinci Seblat National Park (Metusala et al. 2020), as well as N. aristolochioides Jebb & Cheek, which is known Diversity, Ecology and Conservation Status of Nepenthes in West Sumatra Province, Indonesia – Mansur et al. 229 from three locations in the park where it is under threat from collectors (McPherson 2009), underlining the problems of plant conservation even in formally protected areas (Linkie et al. 2010). With the exception of the two latter species, most of the other species described from Sumatra (Hernawati et al. 2022a) and not recorded from the North (Mansur et al. 2022a) or West Sumatra provinces (in this study) are found in the very north of the island in Aceh or in the more central Jambi province. Although rates of land-use change are very high in Indonesia (Margono et al. 2012; Austin et al. 2019), many rare and often endemic species remain in the Sumatran mountains due to the protected status of some localities, combined with their poor accessibility. Many of these species are not in ex-situ cultivation and a stochastic environmental event or agricultural invasion could rapidly cause the extinction of the entire global population of some of these locally endemic species. Conservation needs and responsibilities are therefore extremely high. Further exploration and formal records would add to the quality of existing assessments. Beyond assessing their conservation status, the key threats to the majority of Nepenthes in Indonesia are land-use change and collection for the horticultural trade (Clarke et al. 2018; Cross et al. 2020), so practical conservation methods need to address these challenges that will only be successful with the support of local communities and governments. These fascinating restricted range and threatened Nepenthes species in Sumatra need further study, especially regarding their distribution and population status. A more detailed exploration of the mountainous regions of Sumatra may well find further populations, as we have done here. Figure 3 Nepenthes species recorded from West Sumatra: (a) N. adnata (lower pitcher), (b) N. albomarginata (lower pitcher), (c) N. ampullaria (rosette pitcher), (d) N. bongso (lower pitcher), (e) N. dubia (upper pitcher), (f) N. eustachya (lower pitcher), (g) N. gracilis (upper pitcher), (h) N. harauensis (lower pitcher), (i) N. inermis (upper pitcher), (j) N. izumiae (upper pitcher), (k) N. jacquelineae (upper pitcher), (l) N. jamban (upper pitcher), (m) N. lingulata (upper pitcher), (n) N. longifolia (upper pitcher), (o) N. mirabilis (upper pitcher), (p) N. naga (upper pitcher), (q) N. pectinata (rosette pitcher), (r) N. reinwardtiana (upper pitcher), (s) N. rhombicaulis (upper pitcher), (t) N. singalana (upper pitcher), (u) N. spathulata (upper pitcher), (v) N. talangensis (upper pitcher), (w) N. tenuis (upper pitcher). Photos a & p by Putra, Photos b–i, n, o, q–s, v & w by M. Mansur, Photos j–m by Sahal, Photo t by Sunardi, Photo u by Yusran E. Ritonga. Authorities are noted in Table 1 BIOTROPIA Vol. 30 No. 2, 2023 230 CONCLUSION Our research documented 23 species of Nepenthes in West Sumatra province through direct observation (18 species) and the remainder through herbarium specimens, literature review and second-hand information. Of that total, 18 species are endemic to Sumatra, nine of which are threatened with extinction (2 × VU, 2 × EN and 5 × CR). We examined Nepenthes at one of our study sites (Bukit Malalak) in more detail and compared ecological patterns and processes with those occurring elsewhere. Nepenthes species require further observation, especially regarding their distribution and population, and additional exploration on poorly known Sumatran mountains will lead to new discoveries in this fascinating plant genus. ACKNOWLEDGMENTS This research was funded by grants from Beauval Zoo (France) and Chester Zoo (UK). 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