Nepenthes pudica, a new species from North Kalimantan, Indonesia, is described and illustrated. The species belongs to the N. hirsuta group (sensu Cheek and Jebb 1999) but exhibits some characters that are unique within the group or even within the genus. Above all, it produces underground, achlorophyllous shoots with well-developed, ventricose lower pitchers that form in soil cavities or directly in the soil. No lower pitchers are formed above ground. The main part of its prey are ants, besides other litter- and soil-inhabiting species of invertebrates. A number of infaunal species were found in both aerial and underground pitchers, mainly Diptera and nematodes. Nepenthes pudica is known only from a few neighbouring localities in the Mentarang Hulu district of North Kalimantan, where it grows on ridgetops at an elevation of 1100–1300 m. Its discovery underlines the natural richness of Borneo’s rainforest and the necessity to preserve this important ecosystem with its enormous and still undiscovered biodiversity.

Borneo, carnivorous plant, Caryophyllales, Mentarang Hulu, prey composition, taxonomy, underground trap

Nepenthes L. is a genus of more than 160 species (Golos et al. 2020) primarily distributed in tropical and subtropical Southeast Asia, with centres of diversity in Borneo, Sumatra, and the Philippines. A small number of species occur in outlying areas, including Madagascar, Seychelles, Sri Lanka, northeastern India, southern China, northeastern Australia, and various islands of the western Pacific Ocean (McPherson et al. 2009). The Nepenthes flora of Borneo, with around 40 recognised species, is one of the most species-rich of all. Although the island is still partially covered with extensive primary forest, its area has been rapidly decreasing in recent decades (Miettinen et al. 2011). Commercial logging and subsequent land conversion (mostly for oil palm plantations) drastically reduced the area of pristine old-growth forest from 55.8 Mha in 1973 to 20.6 Mha in 2015 (Gaveau et al. 2016), making the Borneo rainforest one of the most rapidly vanishing ecosystems in the world. The island is botanically relatively well explored in the northern part, i.e. Malaysian Borneo (Sarawak and Sabah) and Brunei, where only remnants of untouched rainforest exist, usually protected as national parks and reserves. In contrast, Indonesian Borneo (Kalimantan) is one of the world’s least explored and most threatened biodiversity hotspots, still with vast areas of relatively intact forest (Raes et al. 2009). However, besides the expansion of oil palm plantations, the announced establishment of the new capital of Indonesia, Nusantara, in East Kalimantan might have a serious impact on the vulnerable biota of Borneo (e.g. Teo et al. 2020). The Nepenthes flora of Kalimantan is poorly known compared to that of Malaysian and Bruneian Borneo, with relatively few modern records. Thus, the new discoveries that have emerged recently after expeditions to certain remote areas of Kalimantan (Robinson et al. 2019; Golos et al. 2020) are not surprising.

Here we describe a new species of Nepenthes from lower montane rainforest in North Kalimantan, Indonesia, which produces well-developed, fully functional and effective underground traps – a strategy as yet unknown in any species of carnivorous plant with pitfall traps. While the majority of carnivorous plants produce their traps above ground or in water, underground traps have up till now been recorded only in the genera Genlisea Benth. & Hook.f., Philcoxia P.Taylor & V.C.Souza and Utricularia L. These genera use three different trapping mechanisms. While Utricularia employs actively working sucking utricles (i.e. Poppinga et al. 2016), Genlisea employs passive ‘lobster-pot’ type traps (Taylor 1991; Płachno et al. 2008). The adhesive leaves of Philcoxia are shallowly buried in sand to receive just enough light to maintain their photosynthetic ability (Pereira et al. 2012). On the other hand, pitfall traps (i.e. traps that rely on gravity) produced from wholly subterranean shoots that have evolved specifically to function underground have not been recorded in carnivorous plants so far (see, e.g. Darnowski et al. 2018).

This study is based on plants found in February 2012 in the Mentarang Hulu district of North Kalimantan province, Indonesia. A total of 17 plants were examined across five different sites. Plants were photographed, sampled and subsequently thoroughly compared with original drawings and descriptions given in protologues of morphologically allied Nepenthes species. Specimens of the Nepenthes hirsuta group were examined in the herbaria BO, K and L (see Suppl. material 1) and the type material was deposited in BO (herbarium codes according to Thiers 2022).

For scanning electron microscopy (SEM), the representative trap parts were fixed in ethanol and later dehydrated and subjected to critical-point drying using liquid CO₂. They were then sputter-coated with gold and examined at an accelerating voltage of 20 kV using a Hitachi S-4700 SEM (Hitachi, Tokyo, Japan), which is housed in the Institute of Geological Sciences, Jagiellonian University in Kraków.

Material for prey investigation was sampled from both underground (tree-root cavities) and aboveground pitchers. The entire contents of five lower pitchers and one aerial rosette pitcher was poured out through a 25 μm sieve, immediately fixed in 4% formaldehyde at circa 80 °C, and stored for 14–21 days, before insects and acarids including also larvae were separated and fixed again. The fine content including nematodes, annelids and organic detritus was transferred into glycerine according to De Grisse (1969) and finally mounted onto wax-glycerine slides and examined. Fixed specimens were identified under a light microscope and documented. All individuals that showed signs of digestion were considered prey. Individuals without signs of digestion were identified and assessed as either prey or infauna based on their biology and present life stages (e.g. larvae were mostly considered infauna). All insect and mite preparations are deposited at the Department of Entomology of Moravian Museum Brno. All the nematodes are deposited in the Department of Forest Protection and Wildlife Management in Brno. Permanent slides of Pristina armata (Naididae) are deposited at the National Museum in Prague, Czech Republic (Schenková and Čermák 2013).

Nepenthes pudica is the first carnivorous species confirmed to use pitfall traps specifically in the subterranean environment. It produces almost exclusively underground pitchers that are well developed and fully functional. Although in some species of Nepenthes pitchers are occasionally reported to develop in plant litter or directly in the soil (Salmon 1993; Nerz et al. 1998; Clarke 2001; Ghazalli et al. 2020), no species that specifically targets this environment to this extent has been documented to date. This is not surprising, as pitchers are generally much larger than other types of traps and are rather fragile due to their hollow character. Therefore, they are generally unsuitable for the soil environment, where considerable pressure is needed to form a cavity. As the pitchers of N. pudica are of a typical size for the genus, they are by far the biggest underground traps among all known carnivorous plants. While the other genera of carnivorous plants that produce underground traps are, due to the small size of their traps, capable of catching only microscopic or very small prey (Seine et al. 2002; Pereira et al. 2012), the pitchers of N. pudica catch prey of the same size as other pitcher plants.

The traps of carnivorous plants are complex and metabolically costly organs that must be produced at the expense of tissues optimised for photosynthesis (Givnish et al. 1984; Pavlovič and Saganová 2015). In pitcher plants, this trade-off often manifests in the separation of primary prey- and light-harvesting structures spatially–e.g. on an intra-leaf level as in most Nepenthes—and also temporally, as in the seasonal production of solely photosynthetic leaves by Cephalotus Labill. and some Sarracenia L., both examples of separation on an inter-leaf but intra-shoot level (McPherson and Schnell 2011; Cross et al. 2019). In N. pudica, this ‘division of labour’ is unusually displayed at the level of the shoots. This strategy is analogous to that of certain strongly shoot-dimorphic aquatic Utricularia, such as U. intermedia Hayne, whose specialised carnivorous shoots penetrate a loose organic sediment while the green stems seek sunlight in clear water near the surface (Adamec 2007).

Each leaf of a typical Nepenthes comprises an entirely photosynthetic lamina-like phyllodium and a predominantly carnivorous and only marginally photosynthetic pitcher (Pavlovič et al. 2007, 2009; Karagatzides and Ellison 2009). The unusual architecture of N. pudica (Fig. 5A) appears to have largely freed it from the phylogenetic constraint of having functional phyllodia and pitchers in close physical proximity, and thereby allowed it to exploit a novel source of prey in the form of the subterranean environment, limiting competition with sympatric congeners. However, this body plan is likely to come with certain costs. Subterranean pitchers, by virtue of having to displace surrounding substrate as they grow, might be expected to have significantly thicker walls and a higher concentration of structural compounds (e.g. lignin) than those produced above ground. Preliminary observations indicate that underground pitchers are indeed markedly thicker-walled and sturdier (M. Dančák & M. Golos, pers. observ.). All else being equal, this would increase their construction costs, partly offsetting benefits from carnivory, and likely dictate longer pitcher lifespans, reflecting a greater ‘payback time’ for recovery of these costs (see Osunkoya et al. 2008). And this does not even consider the additional stem biomass needed for dimorphic shoots. Moreover, the greater separation of the two types of assimilatory organs in N. pudica must presumably necessitate two-way exchange of nutrients and photosynthates over much greater mean distances than in species with typical pitcher–phyllodium pairs (see Osunkoya et al. 2007). All told, the benefit from subterranean carnivory must be significant to make up for these additional costs and this is perhaps the reason this strategy is not seen more widely across the genus.

Figure 5. 

Nepenthes pudica A habit B lower pitcher C infructescence D male inflorescence E detail of climbing stem with a leaf. Drawn by Kateřina Janošíková.

Among Nepenthes, the species that come closest to this degree of shoot specialisation are perhaps those in which pitchers produced in low-light conditions near ground level are borne on crowded, greatly reduced phyllodia (the latter sometimes termed ‘nanophylls’; Cheek 2015). The best known of these, N. ampullaria Jack, additionally produces largely or entirely pitcherless climbing stems (Tan and Wong 1996), mirroring the situation in N. pudica, though the latter’s production of solely carnivorous shoots appears to be unique among Nepenthes and indeed among all pitcher plants. Also of note is the comparatively little-known N. rhombicaulis Sh.Kurata of Sumatra, which rarely if ever produces upper pitchers and has been speculated to target underground prey, though until now its lower pitchers have only been documented to develop within dense moss and detritus rather than being truly subterranean (Salmon 1993; Schmid-Hollinger 1994; Clarke 1997a, 2001). This species, which appears to occupy a similar ecological niche to members of the N. hirsuta group in Borneo, would be a prime candidate for further investigation in this regard.

Since the discovery of Nepenthes pudica, field observations in the Berau region of East Kalimantan (M. Golos, pers. observ. June 2019) have revealed a similar taxon that likewise produces achlorophyllous subterranean shoots bearing nanophylls with reddish pitchers (Fig. 6). This taxon also produces few aerial traps, though it notably differs from the type population of N. pudica in growing at considerably lower elevations. Its precise taxonomic affinities have yet to be determined.

Figure 6. 

Nepenthes sp. with excavated underground traps (bottom left) from a locality in the Berau region of East Kalimantan. Photograph by M.R. Golos.

As was demonstrated above, the prey of Nepenthes pudica consists of various species of soil- and litter-inhabiting fauna. With 25 different taxa, the diversity of identified prey was rather high, which is typical for species growing at higher elevations (Adam 1997). However, ants were the main prey component found in both aerial (subfamily Formicinae) and lower pitchers (subfamily Myrmicinae). At this point, we can assume that N. pudica is predominantly an ant specialist, as are the majority of Nepenthes species.

Consistently with other Nepenthes species, N. pudica harbours relatively numerous and diverse infauna in both types of pitchers (154 individuals and 14 identified taxa). Besides mosquitoes, which are commonly associated with pitcher plants (Vong et al. 2021), larvae of aquatic Diptera (family Stratiomyidae and subsection Acalyptrata) were detected as well. The insect-trapping structures of pitcher plants (especially Nepenthaceae and Sarraceniaceae) frequently harbour dipteran larvae, which utilize the food niche in pitchers (Adlassnig et al. 2011). Members of the family Stratiomyidae are true aquatic organisms inhabiting many kinds of phytotelmata such as tree holes, leaf axils and modified leaves (Greeney 2000); however, their presence in pitchers is not as common in comparison with members of other dipteran families such as Syrphidae, Ceratopogonidae or Chiromidae (Kitching 2000). Rather surprising is the fact that lower pitchers of N. pudica also contained abundant dipteran infauna, including mosquitoes. This indicates that the tree-root cavities from which samples were taken were accessible to the outside-living invertebrates. Therefore, even the hidden lower pitchers can serve as a stable and permanent water habitat (phytotelma) similar to other Nepenthes species or other plants, e.g. unrelated Bromeliaceae (Thorp and Rogers 2015), and play an essential role in the development of these symbionts, especially during dry periods. However, underground pitchers produced in compacted substrate (Fig. 2A) would presumably not be similarly accessible to ovipositing insects.

Nematodes formed the other large group of infauna. Identified individuals belonged to families Aphelenchoididae, Cephalobidae, Diplogastridae, Panagrolaimidae, Plectidae, Rhabditidae (dauer larvae) and Wilsonematidae. The most abundant were members of the genus Pristionchus (Diplogastridae), detected only in the aboveground trap and obviously associated with the main prey, an ant species of the genus Polyrhachis. Species of the genus Pristionchus feed selectively on bacteria and fungi decomposing insect carcasses (Rae et al. 2008), including various genera of ants, e.g. Formica, Lasius and Myrmica (Wahab 1962; Ishaq et al. 2021). The nematodes detected in lower pitchers were members of genera generally living in soil and water environments and feeding on bacteria and fungi decomposing organic material (Bongers 1990). The only exception was the genus Halicephalobus, the species of which are aquatic but occur in extreme environments (Borgonie et al. 2011; Geraert et al. 1988), various phytotelmata (Andrassy 1952; Körner 1954) or as parasites (Stefanski 1954).

Probably the most interesting species living in the pitchers of Nepenthes pudica was the annelid worm Pristina armata (Naididae), which was described from and found so far only in its lower pitchers. For the description and discussion on its relation to N. pudica, see Schenková and Čermák (2013).

The living strategy of Nepenthes pudica can be viewed as an advantageous evolutionary adaptation. As carnivorous plants are highly dependent on prey for organic nutrients essential for reproductive success (Zamora et al. 1997), strong selective pressures may have acted on traits related to prey capture (Ellison et al. 2001). Hence, the potentially strong competition for prey and possible environmental limitations in the forest understorey (e.g. dryness affecting ridgetops) might be avoided by moving the traps underground.

Nepenthes pudica belongs to the N. hirsuta group, which is endemic to Borneo and includes at least two putative close relatives: N. hirsuta Hook.f. and N. hispida. Another two species are sometimes considered members of this group, namely the Bornean N. macrovulgaris J.R.Turnbull & A.T.Middleton and N. philippinensis Macfarl. from the island of Palawan (Cheek and Jebb 1999). However, the recent phylogeny of the genus (Murphy et al. 2020), while proving the close relationships of N. hirsuta and N. hispida, does not support the close affinities of N. macrovulgaris and N. philippinensis, either mutually or to N. hirsuta and N. hispida. Nepenthes hirsuta and N. hispida share a combination of traits that distinguishes this group from the rest of the genus. These are especially the growth form (well-developed rosetted, non-climbing phase), hairy stem, more or less ovoid shape of the lower pitchers, oblique pitcher mouth, ± cylindrical peristome, lid without appendages and flowers usually in pairs (Cheek and Jebb 1999). Nepenthes pudica, while possessing most of these characteristics, shows several unique traits. These are namely a) underground basal shoots (the other species form aboveground basal shoots); b) upper pitchers are only rarely produced in lower parts of the climbing stem; c) lower pitchers are produced exclusively underground; d) the shape of the lower pitchers is ventricose with the lower half ovoid to globose and the upper half infundibular. Another possible member of the N. hirsuta group, Nepenthes leptochila Danser, was described from northern North Kalimantan (Mt. Djempanga; Danser 1928), but this name is usually considered a heterotypic synonym of N. hirsuta (Clarke 1997b; Jebb and Cheek 1997; Cheek and Jebb 2001; Phillipps et al. 2008; McPherson et al. 2009). Nevertheless, the original description mentions several significant differences compared to N. hirsuta (e.g. a well-developed eglandular zone inside the pitchers, glabrous stems and pitchers, and much smaller pitchers) so its identity is at least questionable. Nepenthes leptochila also bears considerable resemblance to N. pudica, especially in being rather glabrous. However, the two taxa differ in all the four previously mentioned characters typical for N. pudica and therefore we do not consider them conspecific. For a comparison of critical diagnostic characters of N. hirsuta (excluding N. leptochila), N. hispida, N. leptochila and N. pudica, see Table 1.

We are grateful to Jiří Schlaghamerský and Jana Schenková (Annelida), Igor Malenovský and Pavel Lauterer (Insecta), Rudolf Rozkošný (larvae of inquilines) and Walter Sudhaus (Nematoda) for help with the determination of prey and to Petr Heřman for comments on Diptera. Kateřina Janošíková kindly prepared the drawing. For facilitating access to herbarium and type materials, we thank Ida Haerida, Yasper Michael Mambrasar, Joeni Setijo Rahajoe and Rugayah (BO); Martin Cheek (K); and Roxali Bijmoer and Nicolien Sol (L). We thank also Kartini Kramadibrata and Muhammad Mansur from Bogor herbarium for help with depositing the type specimens. Alastair Robinson is thanked for valuable comments and suggestions that helped to improve the manuscript. Finally, M. Golos would like to pay tribute to the late Mamed Bin Anwar, without whose generous help the Berau taxon would not be documented herein. Martin Dančák was supported by the internal fund of Palacký University IGA PrF-2022-013.