Nepenthes baramensis ( Nepenthaceae ) – a new species from north-western Borneo

Nepenthes baramensis, a new species from peat swamp and heath forests in north-western Borneo, is described. It is distinguished from related species on the basis of its modified pitchers, which facilitate a facultative mutualistic interaction with Hardwicke’s Woolly Bat, Kerivoula hardwickii, which roosts in its pitchers and may provide the plant with a substantial proportion of its foliar nitrogen. Published on 12 October 2011


INTRODUCTION
Pitcher plants of the genus Nepenthes (Nepenthaceae) are carnivorous, producing jug-shaped leaves that serve primarily as traps for arthropods and other small animals (Clarke 1997). Raffles' pitcher plant, N. rafflesiana Jack (Nepenthaceae), occurs in Borneo, Peninsular Malaysia and Sumatra (Clarke 1997(Clarke , 2001, where it commonly grows in disturbed vegetation and ecotones over nutrient-deficient substrates up to 1200 m altitude. It is very common in northern Borneo and the Malaysian state of Johor in the Malay Peninsula, but patchy elsewhere throughout its range. The plant is a robust climber, producing vines that may exceed 15 m in length. The pitchers of the rosettes and climbing stems demonstrate pronounced dimorphism which enables this species to target crawling and flying arthropods in those parts of the habitat where these prey are most abundant (Moran 1996, Moran et al. 1999, Di Giusto et al. 2008. Nepenthes rafflesiana displays considerable morphological variation (Cheek & Jebb 2001, Clarke 2001, Phillipps et al. 2008 and in Borneo, a sub-specific taxon that produces, narrow, elongated pitchers has been recorded on a number of occasions (Clarke 1997, Phillipps et al. 2008). There are several consistent morphological differences between this elongate taxon and 'typical' N. rafflesiana (Moran 1996, Gaume & Di Giusto 2009, Bauer et al. 2011Fig. 1, 2; Table 1, 2), however, their functional significance has not been addressed in recent taxonomic revisions of the genus (Jebb & Cheek 1997, Cheek & Jebb 2001. Researchers have been intrigued by ecological differences between the 'typical' and elongate forms of N. rafflesiana for some time -these are summarised in Table 1. Notably, Grafe et al. (2011) have demonstrated that the elongate form utilises a unique, facultative nitrogen (N) acquisition strategy, in which Hardwicke's Woolly Bats (Kerivoula hardwickii Horsfield, (Chiroptera: Vespertilionidae)) roost and defecate in its upper pitchers. Bat faeces potentially represents an important nutri-ent resource for the plant: on average, 34 % of foliar N may be derived from this source; in contrast, pitchers of the typical form are not used as roosting sites by bats and faecally-derived N is not present in the leaves . Not all pitchers of the elongate form are host to the bats, and it is possible that the current facultative relationship represents the early stage of a nascent mutualism.
Prior to the research outlined above, the taxonomic importance of the morphological differences between these two taxa was debatable (Clarke 1997, Phillipps et al. 2008. Given that: i) similar degrees of variation exist within some other species (e.g. N. mirabilis (Lour.) Druce); ii) this level of intraspecific variation is not unusual in Nepenthes; and iii) there has been a tendency among taxonomists not to recognise subspecific taxa within the genus (Danser 1928, Jebb & Cheek 1997, Cheek & Jebb 2001, Clarke 2001, there has been some degree of uncertainty about how to treat the elongate form. Furthermore, there appears to be some disparity among ecologists regarding its identity. Moran (1996), Gaume & Di Giusto (2009) and Grafe et al. (2011) referred to it as N. rafflesiana var. elongata Hort., whereas Bauer et al. (2011) used the terms 'elongate form' and 'typical form' to distinguish between them. The name N. rafflesiana var. elongata derives from plants that were raised in cultivation at Kew (Anon. 1897) and has become popular in horticulture as a practical means of distinguishing the two taxa. However, no detailed description of N. rafflesiana var. elongata was ever published and no type is extant at Kew (Cheek & Jebb 2001). Accordingly, there is no evidence that the name N. rafflesiana var. elongata refers to the 'elongate form' of N. rafflesiana from Borneo. Clarke (1997) and Phillipps et al. (2008) discussed this taxon under their comments for N. rafflesiana, mentioning the use of the name 'N. rafflesiana var. elongata' in horticulture, but did not suggest that this was the correct name for the taxon.
On the basis of the findings of Moran (1996), Gaume & Di Giusto (2009), Grafe et al. (2011) andBauer et al. (2011), we contend that the differences between these two taxa are of sufficient importance for the elongate form to be distinguished from N. rafflesiana at specific rank. Although the visible morphological differences between them are comparatively slight, there are additional differences in ontogeny, physiology and chemistry (see Table 1, 2) that are consistent and appear to be involved in divergent N-acquisition strategies. Accordingly, we here describe the elongate form as a new species, Nepenthes baramensis sp. nov.

MATERIALS AND METHODS
Spectroradiometric analysis was carried out on the reflectance characteristics of 22 upper pitchers of N. rafflesiana and 17 upper pitchers of N. baramensis in Brunei, using a model LI 1800 spectroradiometer with an 1800-06 Microscope Receptor/UV Quartz Microscope attachment (Li-Cor Inc., Lincoln, NB). For each pitcher, reflected radiation in the waveband 350 -700nm (ultraviolet to red) was measured from the peristome, which is the site of highest nectar concentration, and an adjacent area of the outer pitcher body below the peristome. All determinations were carried out in indirect natural light, and both readings on a given pitcher were taken within a few minutes of each other, to counter temporal effects on incident light quality. Colour contrast was then calculated for each pitcher, following Dusenbery (1992): where C is the degree of colour contrast (no units), and I p and I b are the mean reflected radiant flux values (W m -2 nm -1 ) for peristome and pitcher body, respectively. Since the reflectance data exhibited high noise: signal ratios in the ultraviolet waveband (< 400 nm), they were therefore smoothed using the LOWESS (locally weighted regression, tension value 0.1) algorithm of the SYSTAT v5.05 package (SPSS Inc., Chicago, IL, USA; Wilkinson 1990). Etymology. The specific epithet elongata was used by G. Beck to describe a specimen of the natural hybrid, Nepenthes × hookeriana Lindl. (Cheek & Jebb 2001) and therefore cannot be applied to this taxon. Instead, we have chosen the specific epithet baramensis, which refers to the Baram River region of north-western Borneo. This region defines the centre of abundance for this species and extends north into the Belait District of Brunei and inland as far as Gunung Mulu National Park in Sarawak.
Terrestrial climber to 6 m tall. Stems terete, up to 8 mm diam. Internodes 0.5-1 cm on rosettes, 10-15 cm on climbing stems. Leaves of rosettes chartaceous to thin-coriaceous, petiolate, the petioles narrow, lacking wings and canaliculate, up to 12 cm long, sheathing the stem for up to 1/2-3/4 of its circumference, not decurrent. Leaf blades oblong, up to 30 cm long, base abruptly contracted into the petiole; apex obtuse, acuminate, tendril insertion simple. Longitudinal nerves 3-5 on each side of the midrib, pennate nerves spreading towards the margins, but often inconspicuous. Tendrils uncoiled, up to 35 cm long. Leaves of climbing stems similar to those of the rosettes but smaller; petioles up to 10 cm long, not winged, sheathing the stem and not decurrent; leaf blades arising gradually from the petiole, oblong, up to 18 cm long, apex acuminate, tendril insertion simple. Lower pitchers up to 20 cm high, up to 5 cm wide, thin-chartaceous, arising abruptly from the tendril, broadly ovoid Complex colour contrast pattern corresponding to insect visual sensitivity Simple colour contrast pattern 3 maxima in ultraviolet, blue and green wavebands 3 Upper pitchers produce insect-attracting fragrance 4,5,6 No fragrance produced 4,5,6 'Effect' differences High diversity of invertebrate prey 1,4,5 Low diversity of invertebrate prey 1,4,5 High prey capture rate 1,5 Low prey capture rate 1,5 Primary prey-trapping structure: peristome 2 (plus viscoelastic pitcher fluid 4 ) Primary prey-trapping structure: epicuticular wax zone 2 No facultative mutualism with bats 7 Facultative mutualism with bats 7  Table 1 List of differences in pitcher characteristics and ecology of N. rafflesiana and N. baramensis. Differences are categorised on the basis of cause and effect. 'Causal' differences include characteristics that have roles in the detectable ecological differences between the taxa (i.e., the 'effects'  in the lower 1/3 with a pronounced hip, cylindrical above, narrowing slightly towards the mouth. Inner surfaces of the ovoid portion below the hip glandular throughout, surfaces above the hip covered in a layer of wax crystals. Two fringed wings, up to 3 cm wide (widest at the base), bearing multicellular fringe elements up to 12 mm long, run from the bottom of the pitcher to the mouth at the front. Mouth round, oblique, concave, rising at the rear into a distinct neck. Peristome sub-cylindrical, up to 8 mm wide at the front and sides, up to 12 mm wide near the apex. Outer surface entire, inner surface with distinct teeth up to 5 mm long; ribs up to 1 mm apart, up to 0.5 mm wide. Lid broadly ovate, base cordate, up to 6 cm long, up to 5 cm wide, lacking appendages on the lower surface. Large, craterlike nectar glands, up to 0.5 mm wide, scattered sparsely to densely around the outer lower surfaces. Spur simple, up to 10 mm long. Upper pitchers 18 -25 cm high, 3 -5 cm wide, thin-chartaceous, arising very gradually from the hanging end of the tendril, narrowly infundibular in the lower 1/3, becoming noticeably broader towards the hip, which is located 1/2 -2/3 of the way up the pitcher; cylindrical above the hip to the peristome. Mouth and peristome similar to the lower pitchers, the latter sometimes with a slight kink at the front. Glandular region covers the entire inner surface below the hip; cylindrical portion above the hip covered with wax crystals. Lid ovate, generally not cordate at the base, up to 6 cm long by 4 cm wide, no appendages on the lower surface. Large, crater-like nectar glands, up to 0.5 mm wide, scattered sparsely around the outer lower surfaces. Spur simple, up to 10 mm long. Male inflorescence a raceme, peduncle up to 12 cm, rachis up to 30 cm, partial peduncles 1-flowered, bracts usually absent, pedicels 12-15 mm long, tepals elliptic, up to 7 by 5 mm; androphore 5-6 mm long, anther head 1.2 by 2 mm. Female inflorescence similar in structure to the male, peduncle up to 12 cm, rachis up to 20 cm, partial peduncles 1-flowered, lacking bracts. Valves of fruits 50 by 10 mm. Indumentum of stem, midribs, lower surface of the leaf blade and inflorescences from base of peduncle to lower surface of the tepals white or grey arachnoid; lower surface of leaf and outer surface of pitchers with minute grey stellate hairs. Other surfaces glabrous. Colour of the leaves and pitchers drying to light green or straw brown, stem white, flowers dark brown. Pitchers on living plants pure light green throughout, or green with red-purple specks on the outer surfaces and lid; peristome green throughout to striped with varying degrees of red and green. Stems whitish grey, leaves dull green.
Habitat & Ecology -Sparsely-distributed terrestrial climber in peat swamp forest, kerangas and kerapah habitats, occasionally locally abundant in disturbed kerangas or along kerangas forest ecotones; below 200 metres above sea level.

b a
Conservation status -Many peat swamp and kerangas habitats in the Baram River region in Sarawak have been cleared in recent years, but similar habitats are still widespread in the Belait District of Brunei and in Gunung Mulu National Park in Sarawak. As long as these areas remain largely undisturbed and protected from forest clearing, we consider this taxon to be at little risk and have classified it as low risk/conservation dependent (LR(cd)) according to the IUCN Red List categories (IUCN 2001).
Notes -It is now well established that the insect trapping capabilities of N. rafflesiana and N. baramensis are significantly different (Table 1). In addition to the production of fragrance, the complex colour contrast pattern of its pitchers (Fig. 2), that appears to be 'tuned' to the ultraviolet, blue and green visual sensitivity maxima typical of its insect prey, allows N. rafflesiana to attract and capture prey at higher rates than N. baramensis. For reasons that are yet to be determined, N. baramensis appears to have evolved towards an alternative supplementary nutrient acquisition strategy (i.e., capturing bat faeces). This strategy is manifested in the loss of characters that specifically attract arthropods, and thus in a syndrome of characteristics that distinguish it from N. rafflesiana. It has not yet been established whether N. baramensis pitchers possess any characteristics that specifically attract K. hardwickii to roost in them, but the cylindrical upper portion of the pitcher provides an ideal physical 'fit' for the bats.
The present study adds to the findings of Clarke & Moran (2011) who noted that several unique ecological relationships between highly-specialized Nepenthes species and various species of animals are facilitated by modifications to pitcher characters. However, these traits either went unnoticed, or were considered unimportant or insufficiently consistent, in previous taxonomic accounts (e.g., Danser 1928, Cheek & Jebb 2001, Clarke et al. 2010. A possible explanation for this is that important ecological interactions with animals may be facilitated by minor modifications to trap characteristics (Clarke et al. 2010, Clarke & Moran 2011, and without the support of ecological data, the taxonomic importance of these traits is easily overlooked (especially when similar traits in other species vary to greater degrees, despite having no known ecological function). Our interpretation of the status of N. baramensis is based on both ecology and plant morphology; by linking the two, we confer taxonomic value on morphological variations that might otherwise seem unimportant.
Many aspects of the functions of the distinguishing pitcher characteristics of N. baramensis, and their relevance to this species' interaction with K. hardwickii, have yet to be investigated in detail. This also applies to other Nepenthes species that have highly specialised interactions with animals: the use of ecological information to address taxonomic questions and hypotheses is still in its infancy with regard to Nepenthes. Although the initial outcomes of this approach are encouraging, we emphasise the need for high levels of scientific rigour in designing and conducting subsequent ecological experiments for this purpose.