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A rosette plant of N. ovata, a species that can climb to a height of 5 m.[1] At this young stage, N. ovata produces ovoid lower pitchers that rest on the ground.

Nepenthes is a genus of tropical pitcher plants comprising woody or subwoody shrubs, subshrubs, lianas, and herbs.[2][3] It encompasses more than 150 species that collectively exhibit a high degree of morphological variability in all major features.[4][5][6]

A typical Nepenthes plant consists of a flexible stem with a spiral arrangement of leaves. Moving outwards from the stem, each leaf consists of a lamina (leaf blade), a narrow tendril, and a water-impounding pitcher (derived from and considered to be the true leaf). The lamina may either be directly connected to the stem or have an intervening narrowing termed a petiole. The pitcher consists primarily of the pitcher cup, a container formed from the expanded leaf into which digestive enzymes are secreted and where prey animals are trapped. A ring of hardened tissue, called the peristome, surrounds the entrance to the pitcher cup. It serves multiple functions, playing a role in prey attraction, capture, and retention, and also provides structural support for the pitcher. A lid, or operculum, usually covers the trap's opening, aiding in prey capture and preventing rain from diluting the digestive fluid within the pitcher or displacing its contents. Like the peristome, the lid lures insects into a precarious position over the pitcher mouth. A small spur is inserted near the base of the lid, on the pitcher's dorsal surface, and this represents the true apex of the leaf. Two fringed wings are often present at the front of the trap; the function of these structures is uncertain. Most species produce at least two distinct types of pitchers; lower pitchers are produced by rosettes and usually rest on the ground, whereas upper pitchers are typically associated with older, climbing stems and are held in the air. Upon reaching maturity, the plant produces an inflorescence in place of a new leaf, with the stem subsequently continuing as a lateral branch. The lateral axes of the inflorescence may bear only a single flower or be secondarily branched and hold up to 40. Nepenthes are the only carnivorous plants that are dioecious, having separate male and female plants. Pollen is dispersed in spiny tetrads (groups of four). Fruits typically each contain several hundred seeds, which in most species are thread-like to aid in wind dispersal. Most Nepenthes have a shallow system of fine, fibrous roots, but a number of pyrophytic species from Indochina produce a well developed rootstock. Many species possess an indumentum of hairs on various vegetative and floral parts; this covering is highly variable in both form and extent.

In most species, the stem and leaves exhibit stage-dependent heteromorphy, their morphology changing markedly when the plant transitions from a low-growing rosette to a climbing liana.[2] This is most clearly seen in the dimorphism of the pitchers. Older specimens may have more than one stem, with additional shoots originating from activated subapical nodes on the original stem (and thus producing a branched stem), from the main rootstock, or from runners, depending on the plant architecture.

Unfavourable environmental conditions can give rise to ecophenes with aberrant morphological features and growth habits. While all Nepenthes are perennials and most experience little or no seasonal variation, an exceptional group of closely related species from Indochina commonly undergoes seasonal dieback and dormancy.

Terminology[edit]

When describing the highly specialised leaves of Nepenthes, the use of terms such as petiole, lamina and tendril can lead to confusion, since the green structure that most resembles a typical plant leaf is actually an expanded leaf base (phyllodium), with the pitcher being a modified leaf blade (lamina) and the tendril an intervening extension of the midrib.[1] The part of the leaf that resembles a true petiole is in fact a narrowing of the leaf base.[2] [see also [7] [8]] In his 1908 monograph, "Nepenthaceae", John Muirhead Macfarlane proposed a practical solution to this naming issue:[9]

That portion which we will subsequently speak of as [...] the lamina or blade is clearly proved, by the above history of seedling leaves, as well as by leaf-embryology, to be but the basal part of the entire lamina. In view however of its relatively extensive green surface, we will for convenience speak of it as the lamina.

B. H. Danser followed this approach in his influential 1928 revision, "The Nepenthaceae of the Netherlands Indies", writing: "[t]he phyllodium of the leaf is usually called leaf or lamina in the descriptive literature and I have followed this practice, as it does not lead to confusion."[10] This use has been continued in all subsequent monographs.[11][12][1][2][4]

Seedlings[edit]

Germination[edit]

Seedlings of N. spectabilis growing on a bare cliff face, showing two distinct developmental stages: the top seedling consists of very small 'pitcher-leaves', whereas the bottom one has already undergone elongation of the laminar midrib and bears distinct pitchers and laminae.
Nepenthes seedlings at various stages of development, from an illustration in J. M. Macfarlane's 1908 monograph, "Nepenthaceae".[9] A: cotyledonary stage, B: seedling with first pitcher-leaves, C: later stage, D: early seedling leaf with a peltate union of the laminar wings, E: tenth leaf from cotyledons (a: petiole, b: lamina, c: pitcher body with wings, d: lid), F: transition leaf between early seedling and adult leaf (references as in E).[9]

[13][14][15][16][17][18][19][20]

morphology/development[21][22][23]

Germination usually takes place within 4–6 weeks of sowing[2] provided the seeds remain in moist conditions, such as on the surface of Sphagnum moss.[9] Where relative humidity is particularly high, seeds may germinate while still in their capsules.[24] Germination in Nepenthes is phanerocotylar (free of seed coat)? and light-dependent.[2][3] The seed coat ruptures along one side as the radicle and hypocotyl elongate. The hypocotyl and cotyledons curve to form a saddle that gradually straightens, freeing the cotyledons from the seed cavity. The radicle steadily lengthens during the first year of growth, reaching around 10 to 15 cm. Numerous lateral rootlets are formed acropetally from its surface. These rootlets grow obliquely downward or even horizontally, as they require good aeration. As a result, Nepenthes seedlings often have shallow root systems.[9] ???[25]

Early seedling growth[edit]

The cotyledonary leaves are green and, like those of the Sarraceniaceae, are retained within the albumin of the seed until it is absorbed.[9] The cotyledons are narrowly oblong to elliptic and measure around 5 mm in length by 2 mm in width.[2] Occasionally three cotyledons may be produced instead of the usual two.[26] They are followed by the growth of around 8 to 10 seedling 'pitcher-leaves', each successive one larger than the previous, which may form a small rosette. These 'pitcher-leaves' are sessile, lack tendrils, and exhibit spiral phyllotaxy,[2] resembling the tubular traps of Heliamphora and Sarracenia species.[9] The first 6 to 8 of these leaves consist of a petiolar rib that is prolonged into a broad laminar midrib whose upper extremity is hollowed out. The ventral surface of the lamina is relatively flat, with the pitcher (which is 2–3 mm long in early leaves)[2] appearing as an appendage on its lower surface. The petiolar rib has a pair of lateral wings that widen as they extend along the laminar midrib. Transverse growth below the pitcher mouth can result in a peltate union of the two laminar wings, although this is not always observed.[9] A peristome is formed by outward and inward growth of the margin of the pitcher mouth. The cellular and particularly the vascular tissue of the pitcher ends in a small spur on the dorsal surface of the pitcher, which is the organic apex of the leaf. A lid is formed between the pitcher mouth and the spur. At this developmental stage, filiform appendages are often present on the margins of the lid and the lamina. In the 8th to 10th 'pitcher-leaf' that is produced, the hollow pitcher body becomes restricted to the distal (upper) portion of the lamina, as it is constricted at its base from the proximal (lower) portion (although in some taxa possessing winged tendrils this union may be observed in mature plants as well). As such, the laminar wings of the distal portion become the ventral pitcher wings and the ventral surface of the pitcher between the wings can be interpreted as the expanded upper surface of the laminar midrib. Elongation of the laminar midrib forms the tendril, which separates the pitcher from the proximal part of the lamina (simply called the lamina in mature plants).[9] The 'hairs' on the upper surface of the lid are gradually lost with age, only being retained in the adult state in a small number of species. Similarly, only a few species have fimbriate leaf margins in the post-seedling stage.

The leaves of very young seedlings typically lack tendrils, the pitcher body being directly fused to the lamina and forming a flattened, leaf-like proto-pitcher. In these tiny rosettes the pitchers often seem disproportionately large and dwarf the laminar portion, but they do not appear to be functional traps at this stage.[27] Occasionally the first true leaf may completely lack a recognisable laminar portion and consist of a large adult-like pitcher on a very short petiole.[26][28]

Plant architecture[edit]

All species begin life as low-growing rosettes like the young N. benstonei pictured (left). Mature plants fall into one of two major architectures: most species have no active subapical nodes, such as the large terrestrial plant of N. madagascariensis with multiple stems (centre), whereas a number of species, most notably N. ampullaria (right), produce a basal 'carpet' of pitchers from activated nodes along the stem.
Nepenthes pervillei7.jpg

Plants start off as low-growing rosettes with a short, erect stem. They are closely beset by leaves and have very short internodes. Rosette plants generally measure around 20–100 cm in diameter.[12] As the plant grows, the internodal length increases. This usually commences 3 to 4 years after germination.[12] In most species, two further stages of stem elongation can be distinguished: a 'short stem' and later a climbing stem.[2] 'Short stems' have longer internodes than rosettes, are up to 2 m tall, and give plants a shrubby appearance. Climbing stems have even longer internodes and result in a liana that often must use tendrils for support.[2] In certain species, such as N. ampullaria, N. flava,[29] N. inermis,[29] N. maxima, N. mikei,[1] and N. tobaica,[1] the transition from the rosette to the climbing stage may be very abrupt, with no appreciable 'short stem' phase.[2] In N. mikei, sequential internodal lengths of 2–3 mm and 10 cm have been recorded.[1]

There are exceptions to this developmental sequence, however; N. argentii, N. campanulata, N. clipeata, N. lamii,[30] N. mantalingajanensis, N. palawanensis,[31] N. peltata, and N. robcantleyi[32] lack a true climbing stage and essentially produce only one type of pitcher,[11][12][4] whereas the weakly climbing stems of N. rajah and N. rowanae rarely reach more than a few metres in length before dying off and being replaced by offshoots from the main rootstock.[33] Nepenthes abalata is also not known to produce a climbing stem.[34]

Stage-dependent heteromorphy[edit]

Most Nepenthes exhibit stage-dependent heteromorphy in their stems and leaves. This is most clearly seen in the dimorphism displayed by the pitchers, but also affects the morphology of the laminae. The pitchers and laminae of short and climbing stems are generally smaller than those of rosettes,[12] and the leaves more strongly petiolate.[2] However, in N. ampullaria, the short and climbing stems produce significantly larger laminae.[2] The cross sectional shape of the stem can also vary with age; in Nepenthes spathulata, for example, 'short stems' are terete, whereas climbing stems are sharply 4-angular.[2] A change in leaf arrangement can also be associated with the transition from a rosette to a climbing plant; in N. maxima and related species the phyllotaxy changes from 2/5 to 1/2.[2]

It is thought that flowering and upper pitcher formation are induced when the climbing stem reaches a certain length.[35] However, the above mentioned non-climbing species flower in the rosette stage, as do members of the Indochinese "N. thorelii aggregate" and ecophenes of many other species.[4]

Production of secondary stems[edit]

Older plants may have more than one stem at a given time. Additional shoots can arise from three different sources: active subapical nodes (resulting in a branched stem), the rootstock, or horizontal runners. Apart from growth after flowering, which requires the production of a branched stem, lateral offshoots from active subapical nodes are uncommon in most Nepenthes species. Production of additional stems from the rootstock, however, is very common. In most Nepenthes the rootstock is quite compact, but certain species possess a large rhizome that gives rise to adventitious stems. Only a few species produce subterranean or terrestrial runners.

Left: A clump of N. ampullaria pitchers formed from an active subapical node on the main stem
Right: Offshoots from an old climbing stem of N. mikei forming aerial rosettes with lower pitchers

From subapical nodes[edit]

Two major plant architectures can be distinguished in mature Nepenthes plants based on the degree of stem branching. Most species exhibit strong apical dominance, whereby the apical meristem inhibits the growth of other meristems further down the stem by means of negative feedback. Subapical nodes usually remain dormant unless the apical meristem is broken off or otherwise damaged. Subapical nodes are also activated following the production of an inflorescence, such that all stems which have previously borne flowers are technically branched (though subsequent growth largely masks this). The most prevalent growth pattern involves the production of a single main stem. At a certain point, this main stem may become branched, and additional stems may be produced from the rootstock.

The second, far less common, plant architecture is best illustrated by N. ampullaria, which often has active subapical nodes in the basal 1–2 m portion of its climbing stems,[2] forming a 'carpet' of pitchers covering the forest floor.[36] Nodes further up the stem may also be activated to produce clusters of lower pitchers many metres off the ground. These are typically held on very small leaves that are dwarfed by the size of the traps.[12] Javanese and some Sumatran populations of N. gymnamphora[note a] have a similar habit of producing clusters of basal pitchers.[1] Nepenthes angasanensis, while not noted for producing such 'carpets', readily forms branched stems with regular offshoots from the leaf axils.[1] Aerial rosettes are common in some populations of N. cf. philippinensis.[37]

In most species, stem branching only occurs with any frequency in the lowermost portion of the stem, where basal rosettes are formed; aerial rosettes are comparatively rare. Nepenthes densiflora and N. lamii are noted for producing basally branched stems, giving them a bushy appearance.[30]

From the rootstock[edit]

A basal rosette of N. bellii bearing lower pitchers, with a trailing climbing stem visible to the right

The architecture of Nepenthes plants is also determined by the structure and development of their underground root systems. Most species produce a central rootstock with multiple stems (which start off as basal rosettes), a strategy best observed in N. gracilis.[1] Other species, such as N. ampullaria and N. rhombicaulis, have an extended rhizome that may give rise to widely spaced adventitious stems.[1]

Unlike normal offshoots, the basal or ground rosettes of N. ampullaria, N. gracilis, and N. gymnamphora do not ordinarily form climbing stems unless the main stem is broken or otherwise damaged.[4] Instead, they typically remain as very short shoots bearing lower pitchers, before eventually withering.[4]

From runners[edit]

An offshoot from a terrestrial runner of N. ampullaria

Certain species produce stolons or runners. These are horizontal shoots that grow at the soil surface or below ground and produce offshoots along their length. This can give the appearance of multiple plants where only one is present. In N. bicalcarata, the runners can exceed 10 m in length, and mature plants of this species are probably the largest in the genus.[12] Nepenthes campanulata spreads rapidly by means of subterranean runners; mature plants of this species often form large clumps with numerous growth points.[4][38]

The combination of regular subapical growth, an extended rhizome, and numerous runners results in mature N. ampullaria forming a 'carpet' of pitchers covering the forest floor.[36] As the species appears to be partially detritivorous, this may be an adaptation to maximise the area over which falling debris can be intercepted.[1]

Environmental effects[edit]

Left: A stunted rosette plant of N. bokorensis growing in an exposed site on Mount Bokor, Cambodia. Plants of this species growing in open areas under direct sunlight are very stunted and often flower when less than 60 cm tall, whereas those found in lower montane forest under sparse tree cover may reach 7 m in height.[39]
Right: A dwarf male specimen of N. alba growing near the summit of Mount Tahan in Peninsular Malaysia. These greatly stunted ecophenes may flower when only 25 cm tall.[4]

The morphology of Nepenthes is largely dependent on the environmental conditions they are exposed to. Lack of light and water can give rise to ecophenes with unusual growth and morphology. Particularly extreme conditions can result in complete dieback of the above ground foliage.

Ecophenes[edit]

Plants growing in marginal habitats may have markedly different phenotypes to those found in more favourable conditions. For example, specimens of [species] growing in exposed sites on ultrahighland mountain tops are often greatly stunted dwarf plants, whereas those found in forest at lower elevations are typical climbing plants. If transferred to a more favourable habitat, such plants would revert to a more conventional appearance. Other species noted for having substantial subpopulations of greatly stunted ecophenes include N. alba,[4] N. bokorensis,[39] N. densiflora,[1] N. diatas,[40] N. gantungensis,[41] N. leonardoi,[42] N. mantalingajanensis,[4] N. murudensis,[27] N. smilesii,[4] and N. ventricosa (on Mount Mayon).[4] However, any species can exhibit abnormal morphology and growth when exposed to less than ideal conditions.

Light is the most important factor with respect to ecophenes. Nepenthes growing in partial shade often exhibit larger leaves and sometimes also larger pitchers. Production of red and purple foliar pigments is typically minimised, resulting in mostly green leaves. In species that ordinarily exhibit an indumentum of hairs, this covering may also be reduced to maximise photosynthetic activity. However, some species are naturally adapted to shady conditions and will not show aberrant growth in such circumstances.[4] Nepenthes aenigma in particular appears to favour deep shade and shows no etiolation in such conditions.[43] Nepenthes hirsuta, N. rhombicaulis, and particularly N. ampullaria, also show a preference for shaded sites, but not to the same degree as N. aenigma.[43]

Plants growing in deep shade may abandon pitcher production altogether in favour of very large, pale green leaves. The foliage of such specimens is often greatly etiolated. They may persist for many years in this state but are unlikely to flower and therefore such subpopulations will eventually die out if conditions do not improve.

Water availability is another important factor. Nepenthes plants that experience drought stress are often stunted as the available moisture is insufficient to support a large amount of foliage. Nepenthes smilesii is a good example of this.[4]

Seasonal dieback and dormancy[edit]

Nepenthes holdenii in the wet season, with dried vines (remnants from the dry season) and fresh shoots visible

The group of closely related Indochinese species that comprise the "N. thorelii aggregate"—N. andamana, N. bokorensis, N. chang, N. holdenii, N. kampotiana, N. kerrii, N. smilesii, N. suratensis, and N. thorelii—experiences a true dry season. These species have a number of special adaptations to cope with this seasonality.[44][45]

A particularly diminutive variety of N. maxima from the grasslands of Central Sulawesi is known to survive seasonal fires. During the dry season its stems may be burned to the ground; new shoots appear in the wet season, originating from the rootstock. It is unknown whether this ecotype possesses an enlarged rootstock such as that found in the pyrophytic species of Indochina.[4]

Stem[edit]

Left: A closeup of the stem of N. chaniana, showing prominent axillary buds and a conspicuous indumentum of long, white hairs
Right: Without surrounding vegetation for support, many Nepenthes species will trail along the ground. Such prostrate stems can stretch for many metres, as in this N. gracilis

Most species have a thin and flexible stem that is insufficiently strong to support the plant's weight without the help of surrounding vegetation.[4] As such, most Nepenthes are scrambling climbers (scandent), using coiled tendrils to gain a hold (N. veitchii is unique in that it uses its leaves to clasp tree trunks). In the absence of surrounding vegetation, most plants are prostrate, growing along the ground.[10] A number of species, most notably N. tenax, produce an erect, self-supporting stem.[4][46]

In most species, mature plants have stems several metres long, but great variation in size is seen across the genus. The species with the shortest recorded maximum stem lengths are N. argentii (30 cm), N. lamii (45 cm), and N. campanulata (50 cm).[4][11][30] Similarly, the little known N. abalata is not known to exceed 50 cm in height.[34] However, ecophenes of some other species may be even shorter at maturity; stunted plants of N. mantalingajanensis, for example, frequently flower at a height of less than 25 cm.[4] Certain ecotypes can be similarly diminutive; particularly small forms of N. maxima found in New Guinea and Sulawesi may flower when only 20 cm tall.[4] On the other end of the spectrum, the longest stems belong to N. bicalcarata and N. gymnamphora,[note a] both of which may reach 40 m.[note a][1][4]

The stem has a tapering form and is usually 1 cm or less in diameter, although it may be up to 3.5 cm thick in N. attenboroughii[47] and N. bicalcarata,[12] and may even reach a basal diameter of 5 cm in some high-climbing species.[10] Its cross sectional shape is mostly circular, two-angled, or triangular;[2] N. rhombicaulis, named for its rhomboid stem, is a notable exception.[48] Rarely the stem may be up to six-angled as in N. northiana or D-shaped as in N. sumatrana.[2]

Development[edit]

Fleshy parts of the stem are generally light green, but may be tinged red, purple or even black in some species.[49][50] After several months, the stem begins to gradually turn brown and somewhat brittle as secondary xylem accumulates. The stem turns woody at approximately the same pace as it lengthens, such that old vines are usually only fleshy in their uppermost one or two metres.[4] Developing stems and leaves are often covered in a dense pubescence, which may be rust-coloured or, more rarely, pale. This conspicuous indumentum is generally caducous, being shed within a few weeks, but may persist for much longer in species such as N. hirsuta.[9] In N. bicalcarata, the stem may be partially hollowed out by ants, with small circular entrance holes cut out along its length.[2]

In one study focusing on plants from Central Kalimantan, Borneo, the stems of N. gracilis and N. reinwardtiana, two fast growing species, were found to have lengthened in one year by an average of 21.74 cm and 13.10 cm, respectively.[51] Nepenthes albomarginata, N. rafflesiana and N. stenophylla all grew less than 9 cm on average in the same time, with N. rafflesiana at one site growing only 3.51 cm (but 7.01 cm at another location).[51] Annual increases in stem diameter were similarly variable, ranging from 0.23 mm for N. gracilis to 1.01 mm for N. albomarginata.[51]

Nodes and nectaries[edit]

Directly above the point of attachment of the leaf to the stem, known as the leaf axil, is a node (axillary bud) bearing a dormant meristem, which may be activated spontaneously or if the stem above is damaged. The uppermost subapical node is the source of new vegetative growth after flowering. It often has the appearance of a small bud or nodule in a shallow crevice and is located up to 1 cm above the leaf base in mature plants.[12] Axillary buds range from inconspicuous to large and spike-like. They are naked, having no scales.[2] Nepenthes are exstipulate (lacking stipules).[2] The portion of stem between nodes, known as the internode, is short in rosettes and increases in length as the plant starts to climb. The internodal distance may be as great as 60 cm[4] in N. hemsleyana (formerly known as N. baramensis and "N. rafflesiana var. elongata").[52][53] However, internodes associated with fertile nodes can be unusually short, even in climbing stems; the internodes separating sequentially produced inflorescences in N. benstonei are an example of this.[2]

Scattered extrafloral nectaries are often present on the stem and may be prominent in species such as N. bicalcarata[9] and especially N. glandulifera.[54] They have the form of small papillae in the middle of a circular or elliptic structure and are often crimson or black in colour.[9]

Petioles and laminae[edit]

Left: A form of N. tentaculata from Sulawesi that produces extremely narrow, linear laminae with upwardly curled margins. The leaves of this species are typically wider with flat margins.
Right: A trio of plants of an undescribed species from Sumatra, with very broad, obovate to oblong leaf blades. Two of the specimens exhibit brownish pigmentation in newly-opened leaves.

Leaves are arranged spirally on the stem, with a phyllotaxy of 2/5 or 1/2.[2][55] The lamina or leaf blade is simple (undivided)[2] and generally linear-lanceolate to spathulate or elliptic in shape,[49] although several species (such as N. robcantleyi and N. truncata) have very distinctive laminar morphology. Seven major lamina shapes can be distinguished: elliptic, lanceolate, linear, oblong, ovate, obovate, and spathulate.[4] Nepenthes clipeata is unique in that its laminae may be almost completely orbicular (circular).[4] In some instances, the two laminar halves on either side of the midrib may differ considerably in size, with one being clearly wider than the other; this is particularly common in N. merrilliana and N. surigaoensis.[4]

The lamina is generally 10 to 45 cm long,[49] but may reach 90 cm in the giant N. bicalcarata.[4] In width, the lamina is usually 1 to 15 cm wide,[49] although the orbicular leaves of N. clipeata may be 20 cm broad[12] as can those of N. macrophylla[27] and N. rajah.[4] Nepenthes glabrata is unusual in that the lamina of rosettes on mature plants may be greatly reduced to the point of being almost absent.[56][2][57] The lamina is generally green to yellow-green in colour, but may even be purple.[49] In certain Nepenthes, such as N. merrilliana[4] and the giant form of N. rafflesiana, the youngest leaves have a reddish-brown pigmentation that is subsequently lost.[12] Some taxa may have a red underside with a green upper surface.[4][42]

Left: The enormous lanceolate to oblong[4] leaf blades of N. bicalcarata are the largest in the genus
Right: Nepenthes truncata is characterised by abruptly truncated laminae[4]

The texture of the lamina is often described as either coriaceous (leathery) or chartaceous (papery),[2] with most species falling under the former. Most forms of N. mirabilis have particularly thin and papery laminae.[1][4] The margins of the lamina are typically entire, but are often fimbriate in N. rowanae,[33] N. smilesii,[4] and, most notably, N. mirabilis; they may reach 5 mm in Thai populations of this species.[4] These fimbriae are attenuated extensions of the laminar surface.[2] Seedlings of many species also display fimbriae on the leaf margins.[2] In certain species such as N. adnata, the margins may be densely lined with hairs.[58][1] The margins may be curled upwards in some Nepenthes, resulting in a V-shaped cross section. This is quite common in N. lamii from New Guinea,[30] N. smilesii and N. thorelii[45] from Indochina, and N. tenax from Australia, and in at least some of these cases may be an adaptation to limit water loss via evapotranspiration.[4] The laminar margins may also be wavy, as in N. undulatifolia[59] and certain forms of N. maxima, particularly those from Sulawesi.[4] Such rippled patterns result from increased cell growth near the edges of the leaf, which causes its thin, planar surface to buckle as it assumes the conformation with the lowest energy state.[60]

Left: An unfurling leaf of N. papuana exhibiting involute vernation
Right: A closeup of an unusual specimen of a giant form of N. rafflesiana with wavy laminar margins bearing conspicuous fringe elements
Estimated leaf half lifetimes of selected
lowland species from Borneo
[61]
Species Longevity, t0.5 (months)
N. ampullaria 14.10 ±3.90
N. gracilis 13.97 ±2.34
N. bicalcarata 9.71 ±1.18
N. albomarginata 7.69 ±1.37
N. rafflesiana (elongated form) * 5.59 ±1.88
N. rafflesiana (giant form) 4.21 ±0.78
N. mirabilis 1.54 ±0.43
* Later identified as N. hemsleyana.[53]
Sample size was ≥80 leaves of each taxon.[61]

Extrafloral nectaries are often present on the petiole and lamina. Their size, distribution, and abundance are highly variable. In N. ampullaria and N. rafflesiana, for example, they are scarce over the petiole and lamina, but a few small papillae may be found on the lower surface of the midrib.[9] In N. khasiana, N. maxima, and N. veitchii nectar glands are more abundant over the petiole and lower laminar surface. They are also present on the upper laminar surface in N. northiana and N. sanguinea.[9] They are most conspicuous and abundant in N. bicalcarata[9] and N. glandulifera.[54]

Leaf development in Nepenthes

Development and lifespan[edit]

Nepenthes laminae exhibit either convolute or involute vernation.[2] The size and shape of the lamina often changes as a plant transitions between rosette and climbing stages.[4] Nepenthes hispida[note f] is noted for its unusual vegetative growth after flowering; the first leaf produced on the lateral stem consists of a small ovate lamina without a tendril.[11][12] Similarly, in N. benstonei, which commonly produces multiple concurrent inflorescences on sequential nodes, the intervening laminae are very short, broadly linear, and do not bear pitchers.[2] Such aberrant growth from fertile nodes is quite common in the genus as a whole, with the laminae often being sessile or more abruptly truncate in the basal portion than usual.[2]

Leaf lifespan varies considerably, with the laminae of N. bicalcarata having by far the greatest longevity among studied species.[62][63][61] Leaves are marcescent, persisting on the stem after withering.[2]

One study from Central Kalimantan, Borneo, found that the number of leaves produced annually ranged from 3.23 in N. stenophylla to 7.57 in the fast growing N. reinwardtiana (though one specimen of N. albomarginata produced 10 new leaves in the same time).[51]

Leaf base and attachment[edit]

Nepenthes leaves are described as either sessile or petiolate, the former being attached to the stem directly by the base of the lamina and the latter having an intervening petiole.

In addition to this, there are 4 major forms of attachment of the stem to either the laminar base or petiole: amplexicaul, clasping the stem (otherwise known as semi-amplexicaul), decurrent, and sheathed.[4] Often leaves exhibit a combination of these, such as an attachment that is both semi-amplexicaul and decurrent. In cases where the leaf base partly encircles the stem, auricles may be present.[2]

In an amplexicaul attachment, typical of N. tentaculata and related species, the leaf entirely or almost entirely encircles the stem. A semi-amplexicaul attachment is one in which the leaf clasps the stem but not for its whole circumference. Finally, in species such as N. chaniana and N. ephippiata, the sides of the leaf surround the stem to form a closed or open sheath.[4]

Left: The stem and leaves of N. northiana, showing the oblong-obovate lamina of this species and the very short internodes typical of young, non-climbing plants. The leaves of this species lack a defined petiole and are characterised as sessile or sub-petiolate.[12]
Right: A rosette plant of N. peltata, a species named for its strongly peltate tendril attachment.[64]

The petiole is the narrow part of the leaf that attaches the lamina to the stem. It ranges in length from 2 to 23 cm[32] and often has a pair of wings that form a short sheath.[49] These wings may be held horizontally (known simply as a winged petiole), obliquely, or vertically upwards as in N. maxima and N. rajah[9] (a canaliculate petiole).[4] The wings may also fold over the adaxial channel to give the petiole a terete appearance, as in N. robcantleyi.[32] The wings may be decurrent down the stem; in N. appendiculata[65] and certain forms of N. hurrelliana[66] and N. maxima[4] the wings extend down the entire length of the internode, while in N. pulchra[67][68] and N. saranganiensis they may even continue into the next internode.[69][4] In Sulawesi forms of N. maxima with wavy laminar margins, the decurrent wings may be highly undulate themselves.[70] Species that lack a defined petiole but nevertheless display a narrowing of the leaf blade may be termed sub-petiolate[12] or pseudo-petiolate.[71]

The two lobes of the lamina can meet at the base in a number of ways. Seven major forms can be distinguished: abruptly contracted, attenuate, auriculate, cordate, obtuse, rounded, and truncate.[4]

Midrib and laminar apex[edit]

The petiole and lamina are characterised by a prominent midrib, which may be strongly concave on the upper surface and even more strongly convex on the underside.[9] In most species, the midrib extends to the apex of the lamina. In these cases the laminar halves may meet in various ways to form pointed or rounded ends. Seven major morphologies can be distinguished: abruptly contracted, acuminate, acute, retuse to emarginate, obtuse, rounded, and truncate.[4] Occasionally the two halves of the lamina may meet the midrib unequally at different points along its length; this is particularly common in N. merrilliana and N. surigaoensis, in which the ends of the laminar halves may be up to 4 mm apart relative to the midrib,[4] and has also been recorded in N. leonardoi.[42] Additionally, a number of species are characterised by peltate laminae, whereby the tendril joins the lamina on the underside, before the apex. This peltate attachment is most pronounced in N. clipeata, N. peltata, N. rajah, and N. undulatifolia; the distance between the tendril attachment and laminar apex can exceed 2.5 cm in all of these species.[4][59][64] In N. clipeata, whose orbicular laminae exhibit the most extreme peltation of all, the tendril emerges one-third to one-half of the way from the apex.[2] Mature plants of many other species can exhibit slightly peltate leaves[12] (termed sub-peltate),[4] but in these cases the tendril attachment is usually within 1 cm of the laminar tip.[59]

Venation[edit]

Nepenthes have camptodromous laminar venation, whereby major veins extend close to the margin, but bend before intersecting it.[2] The venation of the lamina varies between species and may sometimes be diagnostic.[36] These veins (or nerves) are usually visible on the upper surface of the lamina and two main types are distinguished: longitudinal veins and pinnate veins (also called pennate or branching veins).[12] Pinnate veins originate from the midrib or longitudinal veins and form an intricate network of irregularly interconnected reticulate veins. Pinnate veins are often indistinct and rarely diagnostic. Longitudinal veins, however, are often prominent and are important in identifying some species;[12] they are particularly conspicuous in N. mirabilis. They run on either side and approximately parallel to the laminar midrib, usually close to the margin.[2] Longitudinal veins usually originate from the midrib at the base of the lamina, but sometimes they start from a network of lower pinnate veins[10] or pass from the base of the petiole, through its wings, and then spread into the lamina.[9] Longitudinal veins vary in number from 0 to 15 on either side of the midrib, with the innermost ones ending closest?? to the apex of the lamina.[10]

Laminar venation is most prominent in dried specimens and may be difficult to discern in live leaves, particularly if they are thick and rigid.[4]

A giant form of N. rafflesiana with tendrils measuring over 110 cm in length. The transition into aerial pitcher production is thought to be closely tied to flowering. As such, N. rafflesiana which are "not yet ready to bloom" may produce lower pitchers even on higher parts of the climbing stem, necessitating almost 2-metre long tendrils to rest the heavy traps on the ground.[66]
Left: An upper pitcher of N. muluensis, with its tendril coiled around the stem of a neighbouring shrub. Above the pitcher, another tendril is beginning to curl around the same stem.
Right: A deformed upper pitcher of N. albomarginata. In this case, the pitcher cup itself has curled in an attempt to gain purchase around a nearby stem.

Tendrils[edit]

The tendril (also known as the cirrhus[9] or cirrus) is a continuation of the laminar midrib. It is absent in the earliest seedling stages, but is almost always well developed in mature plants.[9] It is unbranched and usually quite uniform in diameter throughout its length,[2] although it may be noticeably thicker towards the base of the pitcher.

The tendril extends from the apex of the lamina to the base of the pitcher. In most species, the tendrils are cylindrical and 1 to 1.5 times as long as the lamina.[49] Nepenthes bellii is noted for its disproportionately long tendrils, particularly those bearing lower pitchers.[4] Tendrils may be up to 110 cm long in N. longifolia[1] and up to 120 cm long on the lower leaves of N. deaniana and N. surigaoensis.[4] Even longer tendrils of 130 cm or more may be produced by N. leonardoi, particularly on leaves bearing lower pitchers.[42] Tendrils, particularly those bearing upper pitchers, are often curled in the middle, forming two or three coils that cling onto surrounding objects for support. Usually the tendrils only remain uncurled in short, non-climbing species such as N. abalata,[34] N. campanulata and N. lamii.[30] Many species which produce short shoots but no climbing stems also have non-prehensile tendrils.EXAMPLES,REF Tendrils are generally yellow-green, but may be tinged with purple.[49]

The tendrils of aerial pitchers are usually coiled in the middle. If the tendril comes into contact with an object for long enough it will usually curl around it, forming a strong anchor point for the pitcher. In this way, the tendrils help to support the growing stem of the plant.[12] Tendrils exhibit great tensile strength, with those of N. rafflesiana capable of holding 6 kg without rupture.[9]

Nepenthes veitchii, while a climbing species, does not utilise curled tendrils for support. Instead, it uses its broad leaves to clasp the trunks of trees.[38] The oldest parts of the stem may die away and roots may grow down from nodes on the stem.[9] An unusual terrestrial form of this species grows in the highland forests of Bario in northern Sarawak. Plants from this area do not climb trees, instead growing horizontally along the ground.[38]

In most species, the tendril connects directly to the lowermost part of the pitcher cup. In the upper pitchers of a number of species, however, the hollow pitcher tube continues past the curved basal portion and for some distance up the tendril.[4] This is most clearly seen in N. epiphytica,REF N. eymae, N. flava, N. fusca, N. jamban, N. ovata, and N. vogelii.[4] Certain species may have winged tendrils.

Nepenthes bicalcarata has specialised tendrils characterised by a swollen and hollowed out base, which forms a chamber that measures up to 6 cm by 1 cm.[9] Ants of the species Camponotus schmitzi make their nests in the this chamber. They access it by chewing a hole through the pitcher wall, possibly utilising the duct of a nectar gland for this purpose.[9]

Pitchers[edit]

Three examples of some of the more unusual pitcher forms: N. aristolochioides (left), which produces hooded traps with an incurved peristome, donward-pointing lid, and often a vertical opening; N. lowii (centre), the aerial pitchers of which are highly constricted in the middle, bear a greatly reduced and indistinct peristome, and have a reflexed lid with bristles on its underside; and N. jacquelineae (right), which has wholly infundibular upper pitchers with a narrow lid and a greatly expanded peristome that is held horizontally.[4]

Pitchers are the hollow traps that form at the ends of the tendrils. They are referred to as ascidia (singular ascidium) in Latin descriptions and some older texts. It is thought that the pitchers of Nepenthes are epiascidiate leaves, meaning they evolved through the infolding of a leaf, with the adaxial (upper) surface becoming the inside of the trap.[72][73][74] The orientation of xylem vessels towards the inside of the pitcher would seem to support this.[75]

Virtually all Nepenthes pitchers share several basic characteristics. Traps consist of the main pitcher cup, which is covered by an operculum or lid that prevents rainwater from entering the pitcher and displacing or diluting its contents.[note a] A reflexed ring of hardened tissue, called the peristome, surrounds the entrance to the pitcher. The pitcher orifice, known as the mouth, is variable in shape. It is often roughly circular or elliptic, but may be triangular or even rhomboid as in N. hamata, N. tentaculata, and related species.[4] The pitcher mouth is apical, except in the domed traps of N. aristolochioides and N. klossii, where it is subapical.[2] Certain specimens of N. eustachya have also been observed to produce slightly hooded pitchers.[1] The orifice usually has an oblique or horizontal insertion, but may also have a combination of the two, being horizontal in the front and rising at the rear to form an elevated region called the neck. Exceptions to this are the two aforementioned domed species, in which the mouth may be positioned vertically.[4][76] Unlike Heliamphora pitchers, which possess a drainage hole or slit to regulate internal fluid levels,[77] the traps of Nepenthes are watertight vessels with the pitcher mouth as the only opening.[4] A pair of fringed wings is usually present on the ventral surface of lower pitchers, although these structures are often greatly reduced or absent in aerial traps. A small spur, considered the true organic apex of the leaf, is inserted near the base of the lid. Apart from these structures, the pitcher cup is usually relatively smooth and featureless on its outer surface, although many species display a prominent hip and some may have conspicuous venation, hair, and nectar glands on the traps.[1] The outer surface may appear matt or glossy. Pitchers are typically held upright, although in species such as N. rajah the lower pitchers may lie reclined on the ground.[12][78]

The number of active pitchers borne concurrently on a single rosette varies greatly between species, from up to 12 in N. micramphora to just 1 in N. diatas.[4] Nepenthes of higher altitudes typically bear fewer live pitchers, although their traps are typically more robust and remain active longer than those of lowlanders.[4]

The upper pitchers of some variants of N. leonardoi may appear almost completely black due to a combination of a purple pitcher surface and brown indumentum[42]

Form and colouration[edit]

The genus exhibits extraordinary variation in pitcher form.[79] Seven major pitcher shapes can be identified: cylindrical, ellipsoidal, globose, infundibular (funnel-shaped), ovate, urceolate, and obconic (amphora-shaped).[4] However, many pitchers represent a combination of these shapes, often having a swollen base and a cylindrical or infundibular upper portion, sometimes with a constriction in the middle (called a waist);[4] this narrowing is most prominent in species such as N. ephippiata, N. lowii, and N. ventricosa.

The cross sectional shape of the pitchers is usually roughly round. Upper pitchers of N. jamban may be perfectly circular in cross section.[4] In some species, the ventral surface between the wings or wing vestiges may be distinctly flattened, resulting in an angled, box-like appearance. Examples of this include the upper pitchers of N. gracillima and N. murudensis.[4] The upper pitchers of N. ramispina are particularly rhomboid in cross section.[4] Nepenthes dubia and N. inermis differ from all other species in having aerial traps with laterally appressed walls that leave almost no gap between the walls in mature pitchers.[1] This modification helps retain trapped prey when the pitchers (which have greatly reduced lids) are overturned by rain. This lateral narrowing is seen to a lesser degree in the upper pitchers of N. chaniana, a species that is otherwise dissimilar to the two aforementioned taxa.[4][80]

Most species have relatively flexible pitchers. In some, certain parts of the traps (often the peristome) may be more rigid than others; in N. edwardsiana, for example, most parts of the pitcher are very flexible, including the peristome ribs, with only the pitcher base, where the digestive zone is located, being rigid.[81] The pitchers of N. ephippiata and N. lowii are atypical of the genus in that they are incredibly tough and rigid throughout, owing to their highly lignified tissues.[82]

Nepenthes pitchers range in colour from ivory white to almost black and may be almost any hue in between, with upper pitchers usually being lighter than their terrestrial counterparts.[4] Plants noted for their wholly white upper pitchers include N. alba and certain variants of N. macfarlanei, N. sibuyanensis, and N. ventricosa.[4] Some Bornean strains of N. rafflesiana may produce both upper and lower pitchers that are entirely white.[4] On the other end of the spectrum, some of the darkest pitchers belong to N. izumiae, N. lingulata,[4] N. nigra,[50] N. robcantleyi,[32] and certain specimens of N. bongso,REF N. leonardoi,[42] and N. rafflesiana.[4] The lower pitchers of N. ramispina are probably the darkest of all.[1] In some cases pitchers may be highly translucent, as in the upper traps of one known population of N. pitopangii.[83] Nepenthes aristolochioides and N. klossii have translucent patches on the rear of their domed pitchers, which are thought to operate as light traps.[4][5][84]

A lower pitcher (left) and an upper pitcher (right) of N. sibuyanensis from Mount Guiting-Guiting on Sibuyan Island in the Philippines. The aerial pitchers of this species, which are rarely produced in the wild, are more elongated than their lower counterparts and completely lack wings.[4] Some are entirely white as in the specimen pictured.[4]

The colour of pitchers on individual plantsCHECK may also vary, according to age, light exposure, soil composition, water chemistry, and drought conditions.[9][4] Many species have traps with reddish speckles or streaks as well as a vividly coloured peristome that contrasts with the rest of the pitcher (although the colour patterns used to attract insects are only visible in the UV spectrum).[2] The waxy zone of the inner surface, often clearly visible through the pitcher opening, may also have prominent pigmentation, sometimes resembling the exterior in its mottling. Colour on its own is typically an unreliable characteristic in identifying Nepenthes taxa as huge variation is often seen within populations, although in certain species, such as N. clipeata, pitcher pigmentation is relatively stable.[4]

Pitcher colour plays an important role in the attraction of prey and some mutualistic organisms (notably tree shrews), and therefore often corresponds to the visual sensitivity maxima of these animals.[85] Colour contrast between the peristome and pitcher cup appears to be particularly important in the majority of species that employ conventional carnivory.[86]

Dimorphism[edit]

Virtually all known Nepenthes produce at least two distinct types of traps: lower pitchers and upper pitchers. Lower pitchers are produced on rosettes and short shoots and typically rest on the ground, while upper pitchers are borne on climbing stems and are normally suspended in the air.[2] Aerial pitchers are generally smaller, narrower and more elongated than their terrestrial counterparts so as to minimise their weight. The tendril is typically attached at the front (ventral surface) in lower pitchers and at the rear (dorsal surface) in upper pitchers.[66][87] In aerial traps, the ventral pitcher wings are often greatly reduced and lacking fringe elements, appearing only as a pair of ribs, or may even be completely absent.[2] Lower pitchers are usually positioned such that their ventral surface faces the stem, whereas upper pitchers usually point away from the stem.[2] In addition, terrestrial pitchers often have darker and more vibrant pigmentation,[4] although this is not always the case; N. leonardoi is noted for having a minority of particularly dark colour variants that produce purplish-black upper pitchers.[42][88] The differences between lower and upper pitchers, while obvious, are usually not great,?? although in some species (such as N. inermis and N. lowii) they may be very pronounced.[4] Because they may be adapted to catching different prey, lower and upper pitchers can also differ in other, more subtle ways (for example, in terms of UV patterns or fragrance).[89]

Left: A tiny upper pitcher of N. ampullaria from Sumatra. Such aerial traps are very rarely produced and appear almost vestigial, often being too small to catch prey.[1] A search by C. L. Wong yielded a single N. ampullaria plant with upper pitchers among thousands of observed specimens.[90]
Right: An intermediate pitcher of N. mantalingajanensis, showing colouration that is typical toward the more exposed summit of Mount Mantalingajan, Palawan. Although it is not in contact with the ground, this pitcher has a ventral tendril attachment and otherwise resembles a typical lower pitcher. Extensive field work involving hundreds of specimens across three habitat types failed to find a single true upper pitcher of this species.[4]

When the plant transitions between lower and upper traps, a small number of intermediate pitchers may also be produced. These often have a tendril attachment at the side,[66] or may incorporate features of both types, such as having well developed ventral wings together with a dorsal tendril attachment. Therefore, the selection of such a specimen as a representative of a species (as appears to have been the case with N. fusca)[12] can lead to taxonomic uncertainty and is avoided by botanists if possible. In species such as N. nigra and N. pulchra, however, intermediate pitchers are very common and appear to be the main trap type produced before plants reach the vining stage.[50][68]

In some species, it is necessary to make a distinction between rosette and lower pitchers. This is especially true for N. sumatrana, whose wholly ovoid lower pitchers differ greatly from the elongated rosette pitchers found on immature plants.[1][4]

There are a few exceptions to the dimorphism exhibited by most species. Nepenthes argentii, N. campanulata,[66] N. clipeata, [12] N. palawanensis,[31] and N. robcantleyi[32] do not have a climbing habit and produce only one type of pitcher (although the position of the tendril attachment may vary).[4] A number of other species only very rarely produce upper pitchers. This is true of, among others, N. ampullaria[91][92][93][90] and N. rajah.[12] Upper pitchers of N. rhombicaulis, which is one of the strongest climbers in the genus, are either extremely rare or not produced at all; the upper stem of this species appears to be primarily used for climbing.[94][95][1] The same seems to be true of some forms of N. gymnamphora[note a][1] and may also apply to the enigmatic N. mollis.[36]

Several Philippine species may also lack true aerial traps, although confirmation of this would require further field work. Observations of N. mantalingajanensis and N. peltata have failed to find evidence of climbing stems or upper pitchers, suggesting that aerial traps of these species are either very rare or absent altogether.[4] It has been speculated that they may produce upper pitchers only in deep shade or if provided with sufficient vegetation to support a climbing stem, as is the case with the closely related N. deaniana and N. mira.[4] Nepenthes veitchii, although a climbing species, lacks the dimorphism seen in other species.[66] Pitcher dimorphism (or lack thereof) may be determined by habitat in some cases; plants of N. densiflora growing in mossy forest are large and produce both types of pitchers, while those exposed to the harsh conditions of open highland meadows (blangs) are very stunted and may have only one type of trap.[1] The lower and upper pitchers sometimes differ so much that they have been mistaken for different species.

Development[edit]

Pitcher development in Nepenthes, from an illustration in J. M. Macfarlane's 1908 monograph, "Nepenthaceae".[9] A: "foliar rudiment showing commencing depression for pitcher cavity B: more advanced stage C: terminal part of leaf D: leaf cut above petiole; a: petiolar base, bc: laminar rudiment continuous with pitcher wings, d: pitcher depression and lid, e: leaf apex, with lateral lobes in 4."[9]
Pitcher development in N. bicalcarata[12]
Phase Period (days) Range (days)
Bud to inflation 19.84 ±1.29 12–41
Bud to opening 27.21 ±0.13 15–52
Inflation to opening 7.37 ±0.59 2–18
Measurements are means ±1 standard error. Sample size was 39 pitchers.[12]
Upper pitcher development in N. neoguineensis, from an inflating bud (left) to a fully formed trap with mature colouration (right)

Development of pitchers.[75][21][61][96][97]

The pitcher starts off as a small bud at the tip of the tendril. Once physiologically activated it begins developing into a functioning trap. The ultimate shape of the pitcher is apparent from an early stage, though with laterally appressed pitcher walls. Initially the pitcher bud is often brown, with the trap subsequently changing colour during elongation. Measurements have shown that the rate of growth is roughly uniform throughout the development process until the lid opens.[75]

The developing pitcher swells as it inflates with air. At this stage, fluid is secreted by glands on the inner surface of the pitcher. The volume of fluid is usually not great; one study found that, upon opening, N. alata pitchers on average contained 12 ml of fluid.[75] The fluid may accumulate as a result of the addition of solutes by digestive glands or transpiration stream through the vascular bundles subjacent to these glands.[75] The inside of the pitcher is sterile until the lid opens after a few days. It appears that digestive enzyme synthesis/secretion and product absorption are temporally isolated, the former occurring while the pitcher is still developing and the latter when the pitcher is open.[98] A brief pause in digestive gland activity occurs immediately before pitcher opening, during which the functional switch from secretion to absorption is thought to take place.[98] Lid nectaries may also play a role in digestive fluid secretion in the sealed pitcher, specifically the discharge of hydrolase and polysaccharide mucilage.[99] During this time, polysaccharide mucilage is also secreted by the peristome nectaries and it is possible that this is involved in keeping the pitcher sealed.[100]

Upper pitchers of N. inermis (left) and related species have very narrow lids that necessitate lateral expansion of the pitcher mouth after opening, whereas plants such as N. pitopangii (right) have similar orifice and operculum dimensions.
Disjunction between the peristome and lid often commences asymmetrically, as in this upper pitcher of N. chaniana

The edge of the lid fits into a corresponding groove in the infolded peristome. It is fused to the peristome by means of interlocking epidermal cells and interwoven trichomes at the lid–peristome junction. The peristome develops by expansion of cells on one side. This forces the lid open and the peristome then begins to unfurl and curl around the pitcher mouth. At this point, the growth rate of the pitcher falls off rapidly.[75] In most species, the shape of the pitcher mouth closely corresponds to that of the lid, and does not change significantly after opening. However, this is not the case in the upper pitchers of N. eymae,[2] or N. inermis and related species, all of which have greatly reduced lids. Prior to opening, the pitcher walls of these species are laterally appressed throughout in order to form a tight seal with the lid. Upon opening, the upper walls 'pop' outwards, forming the characteristic round mouth.[101] Nectar secretion from the peristome[100] and lower lid glands commences shortly after pitcher opening.[99]

Pitchers often become more colourful after opening.

The pitchers of some species, such as N. sibuyanensis, generally develop embedded in the substrate and are rarely exposed to direct sunlight.[102]

Lifespan[edit]

Pitcher lifespans of four Bornean lowlanders[12]
Species Overall lifespan (days) Operational lifespan (days)
N. bicalcarata 234.2 ±66.4 218.6 ±86.9
N. ampullaria 189.7 ±91.7 174.9 ±101.4
N. albomarginata 173.9 ±72.3 167.6 ±79.5
N. mirabilis var. echinostoma 23.9 ±7.1 23.9 ±7.1
Measurements are means ±1 standard error. Sample size was 40 pitchers of each species.[12]
Estimated pitcher half lifetimes of selected
lowland species from Borneo
[61]
Species Longevity, t0.5 (months)
N. bicalcarata 6.01 ±1.85
N. albomarginata 3.46 ±0.98
N. gracilis 2.96 ±0.99
N. ampullaria 2.40 ±0.99
N. rafflesiana (giant form) 1.10 ±0.01
N. rafflesiana (elongated form) * 0.95 ±0.31
N. mirabilis 0.93 ±0.00
* Later identified as N. hemsleyana.[53]
Sample size was ≥80 pitchers of each taxon.[61]

The lifespan of pitchers varies widely between species. The traps of N. mirabilis, for example, live for less than a month on average, while those of N. bicalcarata may persist for over a year. Pitcher longevity may also vary greatly within individual species; pitchers of the typical form of N. rafflesiana last for around 4 weeks, compared to up to 12 weeks in the giant form.[12]

The pitchers of N. ampullaria are relatively long lived, surviving for more than 6 months on average. This species is unique in that it appears to derive a significant proportion of its foliar nitrogen from leaf litter, and it is thought that this trap longevity may be due to the species's reliance on a "slow trickle of nutrients over time".[1]

Peristome[edit]

Left: The upper pitchers of N. inermis are the only ones in the genus to completely lack a peristome. They are also unusual in being wholly glandular on the inner surface.
Right: The peristome of N. izumiae is cylindrical at the front, becoming flattened and broader towards the sides and rear. The largest teeth are located towards the top of the peristome, where they form a double column and are often splayed forward.[4]

The structure surrounding the entrance to the pitcher is known as the peristome. In species with a well developed peristome, it is believed to have a dual function, playing a role in both insect attraction as well as capture and retention.[1][103] Additionally, the peristome serves to strengthen the pitcher cup and provides it with structural support.[4] The peristome is often roughly T-shaped in cross section, with the 'arms' of the T forming two margins, one on either side of the pitcher orifice.[2] These margins may be more or less curled depending on the species.[11][1] The relative widths of the inner and outer peristome sides are highly variable between species; the inner portion of the peristome may account for as much as 85% of its total cross-sectional surface length in N. ampullaria and as little as 20% in N. inermis.[104] Most species have either similarly broad portions on the inside and outside or an expanded outer part only.[105] Plants with a greatly incurved peristome that is significantly broader on the inner side include N. ampullaria, N. aristolochioides, N. bicalcarata, N. klossii, and N. talangensis.[1][4][12] The reflexed peristomes of these species form an 'entrance corridor' that is reminiscent of lobster-pot traps.[106] Such incurved peristomes are generally associated with a reduced or absent waxy zone in the pitcher interior.[104] Narrow, cross-sectionally symmetrical peristomes are thought to be the ancestral state of Nepenthes.[104]

The outer margin of the peristome is typically flat, recurved, or crenellated.[4] In most species it is initially flared but later curls back as the pitcher matures; N. jacquelineae and N. platychila are unusual in that the outer margin of the peristome is held away from the pitcher cup in a roughly horizontal position.[1][107] The peristome is most commonly cylindrical or subcylindrical in cross section, but may also be flattened.[4]

Peristomes range in width from very broad (as in N. robcantleyi, where it may reach 10 cm in width)[32] to very narrow (as in N. gracilis), to almost vestigial (as in N. campanulata).[48] Only the aerial pitchers of N. inermis lack a peristome completely.[1] The peristome in upper pitchers of N. ephippiata and particularly N. lowii is atypical in that it is not identifiably a separate structure from the rest of the trap, instead consisting of a series of raised bumps (flattened ribs) that line the outer edge of the pitcher orifice and emerge directly from its surface.[4][9]

Ribs and teeth[edit]

With the exception of N. platychila, which has an expanded peristome that is almost completely smooth on its upper surface,[107] virtually all species have ribs or corrugations on the peristome. Some specimens of N. jacquelineae and N. reinwardtiana may also lack discernible ribs.[4][2] The ribs may be expanded in some species and this is taken to an extreme in N. edwardsiana, in which the ribs take the form of plate-like flanges and can be up to 2 cm tall.[4][78] The closely related N. macrophylla and N. villosa, also from Borneo, have greatly enlarged ribs as well, although not to the same extent as in N. edwardsiana. The only other species with comparable peristome rib development is N. hamata of Sulawesi. The distance between the ribs is greatest in species with well developed peristomes, reaching 10 mm in N. edwardsiana.[4] Nepenthes mirabilis var. echinostoma is unusual in that its peristome ribs are often expanded into uneven projections that point outwards at different angles.[4]

Left: The peristome of N. fusca from Kinabalu National Park, Borneo. This species has a prominent neck and extremely fine ribs measuring only up to 0.1 mm in height.[4]
Right: The highly developed peristome of N. edwardsiana bears the largest ribs in the genus (≤2 cm tall).[4][78] Its peristome teeth are also some of the longest, reaching 12 mm.[4]

The ribs are often elongated into downward-pointing teeth on the inner margin of the peristome. These teeth may also be well developed, as best exhibited by N. hamata, which has extremely elongated, curved projections, especially in its upper pitchers,[4] where they can reach 16 mm in length.[2] Nepenthes rajah and N. villosa have a particularly intricate peristome structure, with up to two additional rows of teeth present under the main peristome teeth.[4] In the former species, these three lines of teeth are connected by staggered, perpendicular walls, forming two rows of box-like compartments.[2] Nepenthes macrophylla has a similar secondary row of smaller teeth.[108] Marginal nectar glands are present on the inner margin of the peristome, their apertures usually being located between or at the apex of the teeth,[9][2] although some species lack teeth altogether; the marginal glands of the non-dentate N. reinwardtiana are sunken in depressions along the inner peristome edge.[2] Nepenthes ampullaria, which appears to be partially detritivorous, has greatly reduced marginal glands.[1][105][109]ISSUE NO.?

Extensions and projections[edit]

The peristome may be elongated into a neck. This is clearly seen in species such as N. bicalcarata, N. fusca and N. hurrelliana, where the two parts of the peristome are tightly united.[110]NEEDREF In other species, the two peristome lobes may be separated by a gap. In N. rafflesiana, the two sides of the peristome often diverge at the top of the neck, forming a V-shaped gap up to 20 mm wide.[4] In some specimens, this opening may run the entire length of the peristome neck, forming a channel through which insects can pass from the lower surface of the lid directly into the pitcher cup.[66] Nepenthes argentii is unique in that its peristome curves round and continues along the lower surface of the lid for several millimetres.[2][4] In some species, the teeth of the neck are considerably enlarged and form a double column of conspicuous downward-pointing spikes. This is particularly noticeable in N. bongso and related species, where the uppermost teeth are often splayed forward.[4] The peristome neck may be inclined forwards at a considerable angle relative to the pitcher orifice, as in N. eymae.[4]

The peristome may be raised at the front. This feature is particularly prominent in N. rafflesiana and N. sumatrana, where it is often roughly square-shaped.[4] A number of other species display less developed, triangular projections at the front of the peristome, including N. hemsleyana,[52][53] N. bokorensis, N. holdenii,[44] N. longifolia, N. maxima, N. smilesii, and N. truncata.[4]

Nepenthes bicalcarata is unique in that it has a pair of thorns (≤3 cm long) projecting downwards from the top of the peristome.[12] These are derived from the uppermost 10–12 peristome ribs[2] and bear some of the largest nectaries in the plant kingdom.[111][38] They are thought to play a role in prey capture.[112] A somewhat similar peristome modification is found in the two Madagascan species—N. madagascariensis and N. masoalensis—in which each lobe at the top of the peristome is elongated into a prominent triangular point on its inner margin.[4]

Lid[edit]

Left: The very narrow, hastate lid of this N. eymae upper pitcher allows water to freely collect in the trap. This species, like several others with reduced lids, produces very viscous pitcher fluid that aids in prey retention.[4]

Centre: An upper pitcher of N. dubia, showing the tiny reflexed lid. The angle at which the lid of this species is positioned relative to the mouth is only rivalled by N. ampullaria, and almost always exceeds 180°.[1]

Right: The underside of the frilled lid of N. naga, showing a prominent hook-shaped basal crest and the forked subapical appendage for which it is named.[113] A spur with a bifurcate apex is visible directly below the base of the lid.

The lid or operculum is a structure that forms at the top of the pitcher, between the spur and the uppermost part of the peristome, and usually overhangs the pitcher mouth. It is the only major organ to lack a midrib (instead having two main vascular systems), which has led some authors to interpret it as being evolutionarily derived from the fusion of two laminar lobes or leaflets.[2][21][9][105][114][115]ISSUE NO.?[116]see also[117]

The various shapes of the operculum fall under 9 main categories: cordate (heart-shaped), cuneate (wedge-shaped), elliptic, linear (strap-shaped), oblong, orbicular (circular), ovate (egg-shaped), reniform (kidney-shaped), and triangular (including hastate).[4] The lid is usually flat or elevated at the sides (often V-shaped), but may also be vaulted, with the margins curving downwards. The huge vaulted lid of N. rajah is the largest in the genus, reaching 22 cm in length by 26 cm in width.[4] Unusually, it is considerably larger than the pitcher orifice.[2] The lids of some Nepenthes have a distinctly frilled margin. This may be particularly pronounced and even diagnostic in species such as N. naga.[113] The upper surface of the lid may have a raised portion, or basal boss, as in N. robcantleyi.[32]

Position[edit]

In most species the lid is held roughly horizontally and keeps rain from diluting the fluid within the pitcher or displacing its contents. However, this is not the case in the lower and upper pitchers of N. ampullaria, N. attenboroughii,[47] N. macrophylla,[118] and (to a certain degree) N. rajah,[118] nor the upper pitchers of N. dubia, N. ephippiata, and N. lowii, where the lid is held away from the mouth. Similarly, in aerial pitchers of the group of closely related Sumatran species that includes N. inermis, N. jacquelineae, and N. jamban, as well as the group that includes N. eymae, N. fusca, and N. hurrelliana, the lid is so narrow that it only partially covers the trap's orifice, allowing rainwater to collect in the pitchers.[1][4] Most of the species with such unconventional lid forms are either adapted to utilising alternative nitrogen sources (leaf litter in N. ampullaria,[119] tree shrew faeces in N. lowii, N. macrophylla, and probably N. ephippiata,[118][120] and both tree shrew and rat faeces in N. rajah)[121][122] or have extremely viscous pitcher fluid that aids in prey retention (as in N. dubia, N. inermis and related species, and N. eymae and related species).[4][106][123]

Nepenthes aristolochioides and N. klossii are exceptional in that the lid often hangs downwards over the pitcher orifice (which is itself positioned vertically or nearly so).[4] The pitchers of these two species are thought to function as light traps.[4][5][84] On the other end of the spectrum, the most highly reflexed lids belong to N. ampullaria and the upper traps of N. dubia. In the latter, the lid is almost always reflexed beyond 180° relative to the pitcher mouth.[1] In N. ampullaria, the angle varies between populations; plants from Borneo and Sumatra typically have lids positioned 140–190° from the mouth, whereas those from New Guinea may have lids twisted up to 270° away, being pressed up against the pitcher's dorsal surface in the most extreme cases.[4] Nepenthes clipeata is unusual in that its vaulted lid closely surrounds the pitcher mouth, leaving only a small gap.[12] It has been speculated that this may be an adaptation to minimise evaporative water loss from the traps, which often rest against the bare, granitic cliff faces of Mount Kelam and may be exposed to very high daytime temperatures.[12]

Appendages, bristles, and hairs[edit]

Some species have appendages on the underside of the lid, arising from the midline.[2] The most common type of appendage is a laterally flattened basal crest and this is characteristic of B. H. Danser's traditional Regiae group.[2] A triangular or hook-shaped basal appendage is characteristic of, among other species, N. appendiculata,[65] N. burbidgeae,[12] N. chaniana,[80] N. clipeata,[124] N. eymae,[4] N. faizaliana,[125] N. hamiguitanensis,[126] N. hurrelliana (which is noted for being hairy),[110][4] N. izumiae,[127] N. klossii,[128] N. maxima,[11] N. naga,[113] N. ovata,[129] N. pilosa,[130] N. pulchra,[68] N. robcantleyi,[32] N. stenophylla,[131] and certain populations of N. alata,[4] N. bongso,[1] N. boschiana,[4] N. copelandii,[4] N. fusca,[4] N. mindanaoensis,[4] N. peltata,[64] N. truncata,[4] and N. veitchii.[4] Basal appendages are usually covered in many large nectar glands.[2] Certain species have a median ridge or keel (e.g. N. rajah) instead of a prominent crest.[2][105]

Left: The nearly orbicular lid of N. chaniana, viewed from above.
Right: Closeup of the lid–peristome junction in an upper pitcher of N. insignis, with nectar glands visible on the underside of the lid. The lid of this species bears a prominent midline and two distinct lateral veins.[132] A number of large, pit-like nectar glands are concentrated around these veins, forming two groups, one on either side of the midline.[2][102] These glands are transversely elliptic or orbicular and up to 1 mm in diameter. They become smaller and sparser towards the margins and are largely absent from the midline.[2]

The apical lid appendage is less common and may or may not bear glands.[2] It also originates from the midline of the lid's lower surface. A well developed apical appendage is produced by, among other species, N. eymae, N. klossii, and N. maxima, as well as certain populations of N. fusca and, rarely, N. veitchii.[4] In these species the appendage is filiform.[4] Nepenthes robcantleyi bears a short, cylindrical apical appendage.[32] Nepenthes naga and some specimens of N. bongso produce a dichotomous apical appendage.[113] Nepenthes lingulata is exceptional in that it has an extremely large (≤4 cm long in lower pitchers) filiform appendage near the centre of the lid's lower surface.[133] It is believed to function in a similar manner to the peristome spines of N. bicalcarata.[133] Nepenthes appendiculata produces a very large, woody and highly elaborated apical appendage that bears massive nectar glands on its underside.[65] This appendage is particularly pronounced in upper pitchers (c. 3.4 cm long) but, unlike in N. lingulata, its apex does not overhang the pitcher orifice but projects well past it. It likely functions only as an initial lure, rather than being directly involved in prey capture.[65] Lid appendages are often unstable within populations and for this reason should not be considered in isolation when identifying or circumscribing a taxon.[4] The group of related species that includes N. appendiculata, N. eymae, N. fusca, N. hurrelliana, N. klossii and N. maxima often exhibits both a basal and an apical appendage.[4][65] This may rarely be expressed by specimens of N. veitchii as well.[4] Instead of an appendage, some species exhibit a shallow invagination near the apex of the lid's lower surface, the function of which is unknown.[105]

Nepenthes lowii and the closely allied N. ephippiata, both from Borneo, bear densely-packed fleshy cellular bristles on the lower surface of the lid.[12] These bristles are usually most prominent in older and larger plants, and often concentrated near the base of the lid, but may cover its entire underside.[4] A white substance often accumulates amongst these bristles and this is thought to attract tree shrews, which provide the plant with nutrient-rich droppings.[82][118] Nepenthes macfarlanei of Peninsular Malaysia has long, white non-cellular hairs on the underside of the lid,[1][4] which has in the past led to confusion between these otherwise dissimilar taxa.[134][49]

In a number of species, multicellular filiform appendages are present on the upper surface of the lid,[11] though this feature is often unstable and may be absent altogether.[4] These 'hairs' or 'tentacles' are found in mature pitchers of N. hamata (≤20 mm long, often branched), N. muluensis (≤15 mm long, sometimes branched), N. nigra (≤20 mm long, sometimes branched), N. tentaculata (≤15 mm long, sometimes branched), and, more rarely, N. adnata (≤10 mm long, simple).[4][50] These appendages arise from the ends of the lid veins[2] and are mainly restricted to the outer margins of the lid[4] (sometimes only to the rear).[50] Seedling plants of many other species also have these appendages, although in these cases they are lost with age.[9] In addition to these marginal lid appendages, certain taxa, such as Bornean populations of N. tentaculata, may also possess distinct clusters of simple or branched appendages on either side of the spur.[135] Similar structures have been reported in N. undulatifolia, which otherwise lacks lid appendages.[59] In N. hemsleyana, two or more multicellular, filiform appendages (5–10 mm long) are often found on the upper surface of the lid, near the spur, though they are only expressed in lower pitchers.[53]

Waxy coating[edit]

An upper pitcher of N. gracilis with a Polyrhachis pruinosa ant feeding at its mouth. A waxy bloom is visible on the underside of the lid and on the inner surface of the pitcher.

In at least one species (N. gracilis) the underside of the lid bears an uneven covering of wax crystals. This layer is not as thick as, and structurally distinct from, that found in the waxy zone of the pitcher interior, and insects can easily adhere to it in dry conditions. During downpours, however, it functions as part of a trapping mechanism, whereby the impact of raindrops striking the lid causes insects to lose their footing and fall into the pitcher cup below.[136]

Nectar glands[edit]

Nectar glands are often present on the underside of the lid. Like the marginal glands of the peristome, these typically serve to lure insects into a precarious position over the pitcher mouth. They are particularly well developed in N. appendiculata (on the apical appendage),[65] N. jacquelineae and N. peltata, reaching 3 mm in the last species.[64][4] They may also on occasion reach this size in N. klossii and N. lamii.[2][30] The density of nectar glands on the underside of the lid varies greatly between species; for example, in N. monticola and N. vieillardii (two species that were once considered conspecific) they occur at densities of 1400–2000 glands/cm2 and 75–100 glands/cm2, respectively.[2][30][137] The distribution of these nectar glands is variable. They are often concentrated along the midline or absent from the midline and organised in two lateral groups around the lid veins (as in N. insignis).[2] They may also be concentrated towards the lid apex (as in N. jacquelineae),[1] near the base (particularly around an appendage, as in N. robcantleyi),[32] or scattered evenly throughout. The largest nectar glands are often located around the midline, although this is not true of all species.REF Nepenthes lingulata is unusual in that the undersurface of the lid is completely devoid of glands, except for a small group concentrated at the end of its tongue-like appendage.[133] In N. ampullaria, which has a greatly reduced and reflexed lid, nectar glands are very rare and in some cases completely absent from the pitcher lid.[1][2]

Wings[edit]

Left: A pair of N. glabrata upper pitchers, showing the unusual non-fringed wings of this species

Centre: An upper pitcher of N. surigaoensis exhibiting a full complement of wing filaments. The common presence of well developed wings in the aerial traps of this species is one of the features that distinguish it from the closely related N. merrilliana.[4][138][139]

Right: A winged tendril on a lower pitcher of a plant matching the description of N. rafflesiana var. alata. In this specimen the tendril wings are heavily crenellated, unlike the main wings of the pitcher cup, which are curled inwards and bear very long fringe elements.

A pair of fringed ridges called wings (or alae)[4] is often present on the ventral surface of lower traps. Generally, the wings are greatly reduced or completely lacking in aerial pitchers, where they are typically replaced by a pair of ribs or ridges. There may be no vestige of the wings in species such as N. ventricosa. However, three species from New Guinea and its surrounding islands—N. neoguineensis, N. papuana, and N. sp. Misool—produce upper pitchers with well developed wings that often continue along the tendril.[4] The aerial traps of N. mirabilis var. globosa also commonly display this feature,[140] as do those of N. glabrata and N. surigaoensis, although in the case of these latter two species the wings are usually restricted to the pitcher cup.[4] Another plant with winged tendrils is N. rafflesiana var. alata, which has lower pitchers with straight to heavily undulating tendril wings that may be continuous with the lamina.[141][66] Nepenthes lamii generally lacks wings in all its pitchers.[30]

The wings are often fringed with filiform elements, although those of the upper pitchers of N. glabrata usually have an entire margin;[2] this is also seen in some specimens of N. neoguineensis and N. sp. Misool, and often also in the lower pitchers of N. reinwardtiana.[4] The relative length and spacing of the fringe elements is highly variable. They may be webbed and grouped in clusters in some species (as in N. argentii and N. tomoriana, where they are often in groups of 2–4; N. bellii, where they are often in clusters of three; and N. hamata, where they are often in pairs).[2] The fringe elements are typically arranged in an orderly line, all pointing in roughly the same direction, although this is not the case in N. ampullaria.REF Wings are usually straight but may be curled inwards or wavy in some taxa, such as N. mirabilis var. globosa,[140] N. neoguineensis, N. rafflesiana, and N. treubiana.[4] The lower pitchers of N. rafflesiana have probably the most well developed wings of all; they can measure up to 30 mm in width and bear fringe elements up to 20 mm long.[4]

Since the wings are often absent from upper pitchers, for which flying insects constitute the majority of prey items, they were presumed to guide terrestrial insects into the pitcher mouth. However, experimental results do not support this conclusion and their function remains unknown.[142]

Left: A pitcher of N. talangensis viewed from the rear. The spur is visible as an appendage inserted just below the base of the lid. Pitcher venation is not conspicuous in this species.
Right: An upper pitcher of N. neoguineensis with some of its ventral veins highlighted by brown discolouration. Faint dorsal veins are also visible through the pitcher orifice, on the inner surface.

Venation and spur[edit]

Just like the lamina, pitchers often have prominent venation. The veins emerge from the tendril at the base of the pitcher and continue upwards to the peristome as two main systems. The first consists of a pair of major veins on the ventral surface of the pitcher, where the wings join the body. From these, smaller veins pass outward into the pitcher body and into the wings, if they are present. The second system is more abundant and consists of numerous lateral and dorsal veins. When veins from these two systems reach the peristome, small vascular bundles branch off to supply the marginal nectar glands. The main veins curve round the pitcher mouth and converge, giving off two main veins into the lid. Both vascular systems terminate on the dorsal surface, in a small appendage called the spur (or calcar).[9][143]

The spur is considered the true organic apex of the leaf.[9][143][27] It is either flattened or terete[2] and usually inserted very close to the base of the lid, although in certain species (such as N. bicalcarata) it may be positioned some distance below it.[105] The spur is generally filiform and may be simple (unbranched) or, more rarely,[49] bifid, trifid, or fasciculate (with up to 12 branches in N. mikei).[144] The spurs of some species are not easily characterised as either branched or unbranched. Nepenthes aristolochioides, for example, has a broad spur that is unbranched for most of its length, but ends in 2–4 acute points;[2] it has been variously described in the literature as either simple[4] or branched.[145] Although the spur is typically very short, N. spectabilis is noted for its particularly long spur (≤30 mm).[1] Nepenthes attenboroughii and N. palawanensis have exceptionally broad spurs with a maximum basal width of 6 mm and 5 mm, respectively.[4][31] Conversely, the spur may be greatly reduced to the point of being entirely absent or almost so in species such as N. pilosa, in which the structure does not exceed 1 mm in length.[4] Morphologically, the spur appears to be a relatively stable feature within populations and therefore often finds utility as a taxonomic character.[4]

Inner surface[edit]

Cross section of a N. gracilis upper pitcher, modified from an illustration in J. M. Macfarlane's 1908 monograph, "Nepenthaceae",[9] showing the waxy zone (a) and digestive zone (b) as well as trap venation.

The inner surface of the pitcher may be divided into two portions: a waxy zone in the upper part and a digestive or glandular zone in the lower part.[12][146][147] The waxy zone has been variously called the pruinose zone,[49] conductive zone,[21] or conductive/retentive zone.[12] It appears as a whitish or glaucous 'bloom' and functions by causing prey to slip and fall into the digestive fluid, whereas the digestive zone is typically glossy and is involved in the secretion of digestive enzymes and absorption of digestion products.[2][104]

In species with well developed waxy zones the wax crystals generally extend close to the level of the digestive fluid.[104] The boundary between the waxy and digestive zones is sometimes delineated by a rib, known as the hip, which is visible on the outside of the pitcher.[36] Its position varies between lower and upper pitchers (typically being closer to the pitcher mouth in aerial traps), but is usually consistent within a given species, making it a useful taxonomic character in some cases[1] (N. hamiguitanensis, for example, is noted for having a very prominent hip around the middle of its upper pitchers).[126]

Waxy zone[edit]

Waxy zone development and peristome geometry of selected species[104]
Species Waxy zone Inner peristome section Pitcher type (N)
N. adnata Present 54% lower (2)
N. alata Present 43% upper/intermediate (3)
N. albomarginata Present 34% lower (12)
N. ampullaria Absent 85% lower (15)
N. aristolochioides Absent 82% lower (1)
N. bicalcarata Absent 70% lower (13)
N. bongso Reduced 32% lower (4)
N. boschiana Present 39% lower (1)
N. burbidgeae Absent 49% lower (3)
N. burkei Reduced 37% upper (1)
N. danseri Present 43% lower (3)
N. diatas Present 45% lower (3)
N. distillatoria Present 40% lower (2)
N. dubia Absent 45% upper (1)
N. ephippiata Reduced 55% lower (4)
N. eustachya Present 29% lower (1)
N. eymae Reduced 34% lower (4)
N. faizaliana Present N/A upper (2)
N. fusca Reduced 51% lower (3)
N. gracilis Present 35% lower (10)
N. gymnamphora Present N/A lower (3)
N. hirsuta Reduced 51% lower (1)
N. inermis Reduced 20% upper (1)
N. insignis Reduced 43% lower (3)
N. khasiana Present 57% intermediate/upper (5)
N. lowii Reduced 62% lower (9)
N. macfarlanei Present 55% lower (3)
N. macrovulgaris Reduced 31% lower (1)
N. madagascariensis Reduced 54% upper (4)
N. maxima Present N/A upper/intermediate (8)
N. merrilliana Absent 50% lower (4)
N. mikei Present 51% lower (3)
N. mira Absent 60% lower (3)
N. mirabilis Present 49% lower (3)
N. muluensis Present N/A upper (2)
N. murudensis Present N/A lower (2)
N. neoguineensis Present 45% lower (4)
N. northiana Reduced N/A lower (1)
N. pervillei Present 65% lower (2)
N. petiolata Present 40% lower (3)
N. pilosa Reduced N/A intermediate (1)
N. rafflesiana Reduced 53% lower (14)
N. rajah Absent 80% lower (7)
N. ramispina Present 36% lower (4)
N. reinwardtiana Present 37% upper (4)
N. sanguinea Present 26% lower (7)
N. sibuyanensis Absent 54% lower (2)
N. singalana Present N/A lower (2)
N. spathulata Present 32% lower (4)
N. spectabilis Present 41% lower (6)
N. stenophylla Present 34% lower (1)
N. talangensis Absent 78% lower (1)
N. tentaculata Present 57% lower (3)
N. tobaica Present 40% upper/intermediate (10)
N. treubiana Reduced 33% lower (2)
N. truncata Reduced 34% lower (5)
N. veitchii Reduced 47% lower (4)
N. ventricosa Absent 57% upper (6)
N. vieillardii Present N/A lower (2)
The waxy zone was recorded as 'present' when it covered all sides of the inner surface for at least a third of the pitcher's height. Those classified as 'reduced' included examples where the waxy zone was: (1) restricted to a narrow ring that did not extend below the inner margin of the peristome; (2) reduced to a triangular patch in the rear 'neck' region; or (3) only fully developed in certain specimens or ontogenetic stages.[104]

The waxy zone is composed of tiny, detachable wax scales measuring slightly more than 1 μm in diameter.[2][148] It is these scales that stick to the tarsi of insect prey, denying them a foothold on the inner pitcher wall.[105][149][150][151][152][153] The waxy zone is usually more extensive in lower pitchers.[10][2] Generally, the thickness and extent of the waxy zone appears to be greatest in lowland species and inversely correlated with digestive fluid viscoelasticity. This is because the wax is more efficient at trapping ants (which are abundant in lowland areas), whereas viscoelastic fluid is more efficient at trapping flying insetcs (which become more important in highland areas, where ants are scarce).[154] A 2011 study based on cultivated material of 21 species found a mean wax density of 0.124 mg cm−2 (ranging from 0.022 mg cm−2 in N. ampullaria to 0.608 mg cm−2 in N. macrophylla) and a mean total per pitcher wax mass of 1.85 mg (ranging from 0.28 mg in N. ampullaria to 3.40 mg in N. maxima).[154]

A pitcher of N. aristolochioides in longitudinal section, showing the extensive glandular region that covers almost the entire inner surface. This species bears overarched digestive glands measuring 0.2–0.3 mm in diameter, which occur at a density of 200–500 per square centimetre.[145] The peristome is highly asymmetrical in cross section, with the inner section accounting for more than 80% of the total surface length.[104]

Lunate cells have the appearance of modified stomatal guard cells and likely function to deny prey a foothold in the pitcher.[105][1] The pitchers of the group of closely related Sumatran species that includes N. aristolochioides, N. dubia, N. flava,REF N. inermis, N. jacquelineae, N. jamban, N. talangensis, and N. tenuis—which appear to function at least in part as flypaper traps—are often wholly glandular or almost so.[1][133] The upper pitchers of N. epiphytica and [other species] are also wholly glandular.[155] Similarly, in N. bicalcarata and N. ventricosa the glandular region of the pitcher extends almost to the peristome, such that there is little to no conductive waxy zone.[156][157][158] Nepenthes lowii (and N. ephippiata?)REF also lack epicuticular wax.[82] It has been suggested that N. rafflesiana var. typica may be undergoing an evolutionary loss of the waxy zone via peramorphosis.[158][159]

The waxy zone is not discernible in mature pitchers of N. ampullaria[154] (but is sometimes visible in young pitchers)[160] and N. bicalcarata.[157] These two species also lack lunate cells in their pitchers, as these are present in the waxy layer.[161][1][157] The lack of a conductive zone in these species is thought to reflect their specialised nitrogen sequestration strategies. Owing to their reflexed lids, the pitchers of N. ampullaria are often filled to the brim with rainwater (presumably to maximise space for the aquatic pitcher inhabitants central to their detritivorous habit) and would therefore not benefit from a waxy layer. In the case of N. bicalcarata, a waxy layer could impede the movement of its mutualistic ant species in and out of the pitchers.[157]

Intermediate degrees of wax loss are seen in species such as N. inermis, N. lowii and N. rafflesiana (where lower pitchers have a fully developed wax layer that is completely absent from uppers); N. densiflora and N. fusca (whose aerial pitchers retain only a small patch of waxy covering); and N. burkei, N. northiana and N. treubiana (in which both pitcher types bear only a small triangular area of wax crystals in the upper rear portion of the inner wall).[104]

Reduction or absence of the waxy zone is correlated with wide peristomes and ones having a disproportionately long inner slope, suggesting that most species rely heavily on only one of two trapping mechanisms: wax crystals on the inner pitcher surface preventing prey adhesion or a wetted peristome causing prey 'aquaplaning'.[104] A well developed waxy zone is thought to represent the ancestral state of Nepenthes.[104]

Nepenthes reinwardtiana is known for often having a pair of symmetrical 'eye spots' on the inner surface of its pitchers, usually positioned around 2 cm below the top of the peristome in mature traps[12] (although they are sometimes found deep inside the pitcher).[4] These 'eye spots' appear darker than the rest of the inner pitcher wall since they lack the wax plates of surrounding tissues.[4] Their function is unknown, although they are occasionally seen in the pitchers of other species. These 'eye spots' have also been observed in pitchers of N. angasanensis, N. gracilis, N. mikei, N. sanguinea, N. stenophylla, N. tentaculata, and N. tobaica.[12][1][4] In most of these species, the spots are displayed very rarely and only occur on individual pitchers.[12] However, populations of N. tobaica south of Lake Toba, Sumatra (particularly those from Mount Sorik Merapi and the road from Sibolga to Tarutung) regularly possess these eye spots.[1] Nepenthes reinwardtiana itself occasionally exhibits pitchers with three spots, only one, or none at all.[2][27]

Left: A pair of N. reinwardtiana pitchers, showing the characteristic 'eye spots' of this species, which may be up to 5 mm wide.[2] The 'eye spots' on the right are typical, while those on the left appear to be malformed.
Right: An upper pitcher of N. pitopangii from Sulawesi. In this species, the digestive glands form a conspicuous band of black dots around the waterline of the pitcher fluid.[4][162]
An upper pitcher of N. talangensis, showing the inward-sloped peristome of this species

Digestive zone[edit]

The digestive zone is often more extensive in upper pitchers and some of these traps may be wholly glandular[10][2] (as in N. attenboroughii and N. inermis).[4] The extent of the digestive zone and the number of digestive glands can vary greatly within individual species, likely as a result of differing ecological factors.[137] Digestive glands typically appear as black dots no more than 1 mm wide,[4] although their dimensions are quite variable.[2] The size of the lowermost digestive glands may be diagnostic in certain regions.[49][2] The concentration of digestive glands can be as high as 6000/cm2 in N. stenophylla.[note b][131][49] The density of glands is usually much lower, however; the pitchers of N. rafflesiana are more typical, having 1200 glands/cm2 or more and sometimes in excess of one million glands total.[4]

Size[edit]

Tallest pitchers based on published reports
Species (type) Pitcher type Maximum height Maximum width
N. edwardsiana upper >50 cm[78] 15 cm[12]
N. sanguinea (Mount Benom) 50 cm[163]
N. hemsleyana * upper 48 cm[4] 17 cm[4]
N. merrilliana lower 45 cm[4] 16 cm[4]
N. pulchra upper 42 cm[68] 7 cm[68]
N. rajah lower 41 cm[164] 20 cm[4]
N. northiana lower 40 cm[27] 15 cm[12]
N. boschiana (Mount Sakumbang) upper 40 cm[4] 10 cm[4]
N. truncata upper 39 cm[4] 11.5 cm[4]
N. rafflesiana (giant form) lower 38 cm[4] 19 cm[4]
* Previously known as N. baramensis and "N. rafflesiana var. elongata".[53]
Largest pitchers based on published reports
Species (type) Pitcher type Maximum volume Maximum fluid content
N. rajah lower 3.5 litres[4] 2.5 litres[78]
N. merrilliana lower 3 litres[4]
N. palawanensis lower 2 litres[165]
N. attenboroughii lower >1.5 litres*[4]
N. bicalcarata lower >1 litre[12]
N. rafflesiana (giant form) lower >1 litre[12]
N. deaniana lower 1 litre**[4]
N. northiana lower >900 ml[4]
* Maximum recorded volume; probably produces pitchers in excess of 2 litres.[4]
** Maximum recorded volume; probably produces pitchers in excess of 1.5 litres.[4]

The size of pitchers can be quantified in a number of ways, including in terms pitcher height, pitcher volume, and pitcher fluid content. The natural fluid content of pitchers is not necessarily indicative of their size, however, as it is often dependent on rainfall and the positioning of the lid over the pitcher orifice. As such, total pitcher volume is a better measure of relative size. When determining pitcher height, usually only the pitcher cup is taken into account (often measured from the pitcher base to the spur or the highest point of the mouth),[104][166] excluding the lid, which may be held in various positions and thus exaggerate the trap's size.

Left: A rosette pitcher of N. tenuis with a human thumb for size comparison
Right: A tiny lower pitcher of N. argentii

Smallest[edit]

The smallest mature pitchers are likely to be those of either N. argentii or N. tenuis, both of which are not known to exceed 5 cm.[4][167][129] The terrestrial pitchers of N. argentii measure up to 4 cm by 2.8 cm, although they are usually much smaller.[4] Pitchers produced on higher parts of the stem are more elongated and may reach 5 cm in height by 2.5 cm in width.[4] The lower pitchers of N. tenuis reach 3.5 cm in height by 2.5 cm in width.[4] The upper traps are slightly larger, growing to 4.5 cm by 3.5 cm.[4]

Nepenthes ampullaria is another contender; the extremely rare upper pitchers of this species grow to only 5 cm high by 2 cm wide.[1][4] The aerial traps of N. ampullaria populations from Singapore and the Malaysian state of Johor appear to be particularly diminutive, measuring only up to around 2 cm by 2 cm and apparently being non-functioning.[1][2][168]

Other small traps include those of N. bellii,[169] N. micramphora,[4][170] and certain miniature varieties of N. maxima from New Guinea and Sulawesi.[4] The Sulawesi species N. pitopangii has also been reported to produce very diminutive pitchers, although all measurements are based on the very small number of known individuals.[162][83]

Largest[edit]

The longest recorded N. rajah pitcher, measuring 41 cm[164]

The lower pitchers of N. rajah are probably the largest in the genus in terms of both maximum volume and average size.[4] They have a maximum volume of more than 3.5 litres,[4] and can hold up to 2.5 litres of fluid.[78] More typically, mature pitchers have a volume of 1–1.8 litres and hold 600–1000 ml of fluid.[4] They reach dimensions of 41 cm in height[164] by 20 cm in width.[4] The pitchers of the giant form of N. rafflesiana[12] as well as those of the Philippine species N. attenboroughii,[47] N. merrilliana, and N. truncata may rival those of N. rajah in size.[27] Similarly, the terrestrial traps of N. northiana may be up to 40 cm tall.[27] The Philippine island of Palawan appears to have the highest concentration of giant-pitchered species, with N. attenboroughii, N. deaniana, N. gantungensis, N. mira, and N. palawanensis among its inhabitants.[5][171]

The tallest pitchers may be those of N. edwardsiana, which can exceed 50 cm in height by 15 cm in width.[12][78][4] In 1862, Spenser St. John recorded one pitcher of N. edwardsiana measuring "twenty-one inches and a half long", or almost 55 cm.[172] The upper pitchers of N. edwardsiana can naturally contain in excess of 400 ml of fluid.[4] The length record of N. edwardsiana may be challenged by a particularly large form of N. sanguinea from Mount Benom in Peninsular Malaysia, which is known to produce pitchers up to 50 cm high.[163]

Nepenthes rajah.pngNepenthes rafflesiana giant upper pitcher.jpgNep northiana.jpgAttlwr.jpgNepenthes edwardsiana entire ASR 052007 tambu.jpgN.alisaputrana huge LP.jpg
From left to right: (1) a giant lower pitcher of N. rajah, which produces the largest traps in the genus in terms of volume; (2) an upper pitcher of the giant form of N. rafflesiana measuring around 45 cm; (3) a lower pitcher of N. northiana measuring 40 cm, around the maximum size for traps of this species; (4) a large pitcher of N. attenboroughii; (5) a large upper pitcher of N. edwardsiana; (6) a giant lower pitcher of N. × alisaputrana

A number of natural hybrids also produce very large pitchers, possibly as a result of heterosis (hybrid vigour). These include N. × trusmadiensis (N. lowii × N. macrophylla)[173] and N. × alisaputrana (N. burbidgeae × N. rajah),[174] both of which have traps reaching 35 cm in height.[27][78] Pitchers of similar dimensions may be produced by certain man-made hybrids.[175]

The large pitcher size of some of these species allows them to occasionally catch vertebrate prey.[4][172][176][177][178]

Inflorescence[edit]

Left: A developing inflorescence of N. maxima, showing the terminal nature of the growth, with the stem subsequently continuing as a lateral branch of the original stem

Centre: Male inflorescences of N. mirabilis from Hong Kong????, showing their sequential bottom-to-top development

Right: A male N. ampullaria plant with three inflorescences at various stages of development. The many-flowered pedicels of this species's paniculate inflorescence can be seen.
Detail of the growth point of a N. palawanensis rosette, showing the point of emergence of the peduncle
Nepenthes rosea from Peninsular Thailand is unusual in that it sometimes produces a rosette along the middle of the peduncle. This adventitious growth was found in around a third of the 300 or so plants seen in the wild.[179]
A flowering specimen of N. smilesii from Cambodia with an exceptionally long peduncle

Compared to the pitchers, the floral structures of Nepenthes are rather inconspicuous. Flowers are produced on an inflorescence that arises from the apex of the main stem. Although it is terminal, the inflorescence often appears to be a lateral growth due to the development of a side stem in the axil of the uppermost leaf.[10][2] The inflorescence is erect, but often exhibits some curvature.[4] It holds the flower cluster high above the rest of the plant and often surrounding vegetation as well;[note d] this may help to avoid a pollinator–prey conflict.[180] The length of the inflorescence is highly variable, ranging from 9 cm in N. lingulata[4] and N. murudensis[12] to 213 cm in N. robcantleyi.[32] Large inflorescences may be very robust, greatly exceeding the stem in girth; the inflorescence of N. northiana can have a diameter of up to 10 cm, flowers included.[2][4] Indochinese Nepenthes generally produce rather slender and dense clusters of flowers borne on long peduncles, an arrangement that may have evolved to minimise wind resistance.[34]

Structure[edit]

The main axis of the inflorescence consists of two parts: a peduncle and a rachis. The peduncle is the basal unbranched portion, while the rachis is the upper portion bearing lateral axes. Two types of inflorescences are distinguished based on the degree of branching of these lateral axes. The inflorescence is either a [racemose panicle] simple raceme or, less commonly, a compound raceme (paniculoid thyrse[2]). The former is often simply referred to as a raceme or racemose inflorescence, while the latter is called a panicle or paniculate inflorescence, although some authors consider the former terminology to be incorrect.[note d][note e] Paniculate inflorescences are mostly associated with the less derived species native to the outlying areas of the genus's geographic range.[4] [mention rachis/axis] At least ten species produce a paniculate inflorescence: N. ampullaria, N. bicalcarata, N. danseri, N. distillatoria, N. madagascariensis, N. masoalensis, N. neoguineensis, N. paniculata, N. pervillei, and N. tomoriana.[2][4] It is possible that N. sp. Misool (which is very similar to N. neoguineensis and may be conspecific with it) also has a paniculate inflorescence, but its floral structure has not been documented.[4]

Inflorescences are ramified into pedicels, which hold the individual flowers. In racemes, the pedicels are generally one-flowered or furcate and two- or even three-flowered (in which case they are often called partial peduncles), while panicles can have anywhere from 3[49] to 40[2] flowers per pedicel, although usually up to 12.[4] A single inflorescence can bear both simple and branched lateral axes,[4] with the lower pedicels often bearing more flowers than those higher up the rachis.[27] The total number of flowers on a single inflorescence can range anywhere from 6 to 300, although N. adnata may have as few as 4.[2][note d] The main axis of the inflorescence exhibits indeterminate growth, with flowers developing sequentially from the base towards the growing tip (acropetally).[2]

Some species have bracts arising from the rachis or partial peduncles, or bracteoles arising from the pedicels.[181](check ref)[1] Plants lacking these structures are termed ebracteate and ebracteolate, respectively.[2][3] During the normal course of development, the pedicels lengthen substantially, usually raising their flowers some distance away from the basal bracts.[182] Nepenthes lavicola, however, has very prominent bracts that often overarch even mature flowers and may be up to 7 cm long at the base of female inflorescences.[183] This species is also unusual in that it bears up to two bracts per pedicel or partial peduncle.[183] Nepenthes palawanensis is unique in having ciliate, decurrent, bract-like outgrowths on the rachis of the male inflorescence.[31] The inflorescence of N. leonardoi often bears a vestigial leaf below the rachis.[42] Nepenthes rosea is noted for its peduncle-borne rosettes, which are found on around one in three inflorescences.[179] This species also unusual in that it sometimes produces an enlarged bract, in the shape of a miniature leaf, near the base of the rachis and associated with a single flower.[179]

Inflorescences of both sexes have the same basic structure, although those of female plants are generally somewhat shorter and more robust, having a longer peduncle and bearing fewer flowers on stouter pedicels.[10][2][182] This is not always the case, however; in some species, such as N. gracilis, the female inflorescence may be larger.[1] Nepenthes chang is unusual in that the morphology of its inflorescence differs greatly between sexes; male flowers are borne on two-flowered partial peduncles that often bear short bracts, whereas female flowers are borne solitarily on ebracteate pedicels.[184]

Nepenthes benstonei is one of the few Nepenthes species known to produce multiple inflorescences concurrently on a single stem.[185] Two to three are usually produced, originating from sequential nodes at the top of the stem. This unusual reproductive habit has also been observed, although much more rarely, in N. alba, N. ampullaria, N. attenboroughii, N. rigidifolia, N. sanguinea, and N. thai.[1][4][71] Nepenthes philippinensis takes this to an extreme; mature plants of this species frequently bear up to 100 inflorescences concurrently, with the most ever recorded being around 190 on a single male plant.[4] Since N. philippinensis can bear up to 120 flowers on each inflorecence, it also probably produces the most concurrent individual flowers of any species in the genus.[4] Nepenthes attenboroughii is known to occasionally produce bifurcate male inflorescences, which hold nearly twice the normal number of flowers.[4]

The lifespan of inflorescences has been little studied. One investigation found that the inflorescences of N. rajah, N. villosa, and the natural hybrid between these two species—N. × kinabaluensis—live for up to 3 months, with 0–6 flowers opening daily.[186][2] A study of N. lowii and N. villosa floral morphology found that male inflorescences wither shortly after anthesis, whereas female inflorescences persist in an upright posture, turning partially woody with age.[182] The withered inflorescences of N. attenboroughii appear to remain attached to the stem for a number of seasons; up to five inflorescences of various ages (both living and dead) may be present on a single plant.[187]

Left: A mature male inflorescence of N. smilesii from Cambodia, showing four distinct stages of floral development: closed buds, freshly-opened green flowers prior to anthesis, mature red flowers, and older black flowers.

Centre: Male flowers of N. mirabilis from Hong Kong????, showing details of the crowded anthers and the one-flowered pedicels typical of this species[2]

Right: A sparse female inflorescence of N. pervillei

Flowers[edit]

All Nepenthes species are dioecious, which means that individual plants produce only functionally male or female flowers[note e] and self-pollination cannot occur. As such, female flowers lack an androecium, while male flowers lack a gynoecium.[2] Sex in Nepenthes is thought to be genetically determined.[188]

Perianth[edit]

The perianth lacks petals, consisting of 4 undifferentiated sepals (often called tepals).[2][49] These tepals are imbricate and have been interpreted as either a single whorl of 4 or two whorls of 2.[2] Rarely the perigone may be 3-, 5-, or 6-merous.[10][note d] An odd number of tepals is particularly common in N. pervillei, which sometimes has only 3.[4] Tepals vary widely in morphology and may be elliptic, lanceolate, oblong, ovate, or rounded,[4] with those of female flowers often being narrower.[9][10][182] During anthesis, they are typically concave on their adaxial (upper) surface, forming a receptacle for nectar; they later become reflexed.[182] The tepals may bear persistent hairs on their margins and abaxial (lower) surface.[182] The tepals are patent (unobstructed) and may be free or basally united.[2] Nepenthes argentii is unusual in that its tepals do not open completely as is typical of other species, instead closely surrounding the androecium or gynoecium.[4] The tepals may be decussate, with the outer (lower) pair usually being slightly larger than the inner pair.[182] In unopened flowers, where all four tepals are bound by a multitude of hairs, the outer ones may overlap the margins of the inner ones.[182] Male buds may be globose and female buds more ovoid.[182]

Large, sessile nectar glands cover at least half of the adaxial surface of the tepals.[2] Their distribution and relative dimensions vary between species; they may be roughly uniform in size and restricted to the central portion (as in N. lowii), or gradually decrease in size towards the margins where they form a continuum with the marginal trichomes (as in N. villosa).[182][189] These floral nectaries are similar in structure to the extrafloral nectaries found in pitchers.[182] They produce copious amounts of nectar which coats them entirely.[2] In one studied species, N. gracilis, nectar secretion was found to occur in the early evening.[190][2]

The colour of the tepals is variable; they are usually green, yellow, orange, red, pink, or brown on their adaxial surface.[2][4] In some species, such as N. andamana,[191] the colour differs between mature male and female flowers. The colour may also vary with age, usually changing from green or yellow to orange or red. This is commonly associated with anthesis in male flowers,[4] and has been recorded in, amongst others, N. andamana,[191] N. aristolochioides,[4] N. bicalcarata,[4] N. chang,[184] N. lowii, N. robcantleyi,[32] N. thorelii,[45] and N. villosa.[182]

Nepenthes flowers are often fragrant owing to the nectar production of the tepals.[182] Their scent can range from sweet to musty or fungus-like.[27] Species noted for a "slightly musky or foetid" odour include N. fusca, N. macfarlanei, N. rajah, N. reinwardtiana, N. villosa, and N. × kinabaluensis.[2][186][192] Nepenthes hirsuta is said to have a "faintly sweet" scent, whereas the flowers of N. mirabilis are reportedly similar in smell to mouse droppings or acetamide.[2] Similarly, those of N. thorelii have a "sweetish, murine scent".[45] Nepenthes leonardoi is noted for its particularly strong and distinctive odour.[42][88] The smell is often strongest in male flowers and at night.[4] However, the flowers of some species produce no appreciable odour.[66]

Androecium[edit]

Floral diagram based on N. distillatoria, from J. M. Macfarlane's 1908 monograph, "Nepenthaceae".[9] A: male flower, B: female flower, n: stigmas viewed from below, with the upper part of the ovary in transverse section, revealing the four cells.[9]

Male flowers usually bear 4 to possibly 12 stamens.[2] They are synfilamentous; that is, the stamen filaments are united into a single column, the androphore. The anther heads are initially sessile within the flower bud, but are gradually elevated by the growing androphore during flower opening.[182] In some species, the androphore may lengthen more than twofold during its functional life (after flower opening);[50] in mature flowers it is usually about as long as the tepals.[4]

Anthers are closely packed, forming a subspherical anther head.[2] They may all be erect and arranged in 1 to 3 dense whorls,[2] or form one whorl and an apical group,[10] as in N. villosa.[182] The anthers are typically tetrasporangiate; that is, the microsporangia are grouped in fours. This makes it possible to distinguish individual anthers despite their crowded nature.[182] The number of anthers is highly variable, even on individual inflorescences. Basal flowers often have more stamens than those higher up the rachis; in N. lowii and N. villosa, their number can range from only 3 in the upper parts to as many as 7 near the base.[182] Nepenthes khasiana is reported to have 20–30 bisporangiate anthers.[193]

Pollen is released by extrorse dehiscence of the anthers, whereby the outward facing locules open by means of longitudinal slits.[2] The anther head turns yellow upon dehiscence,[2] with the exposed yellow pollen remaining in its opened sacs for some time.[182] In N. macfarlanei, pollen release typically occurs between 6 a.m. and 2 p.m., but can continue until 5 p.m. (all times local).[192][2] Pollen is dispersed in tetrads (groups of four) and has a distinctive microstructure.[2] As far as is known, all Nepenthes are entomophilous (insect pollinated).[4][2]

Gynoecium[edit]

Female flowers have an ellipsoidal, ovate, or spherical superior ovary, which is typically held on a short stalk called the gynophore.[2][4] The anthetic gynoecium may be covered in a dense indumentum of coarse, ferruginous hairs.[182] Most of these hairs are caducous, being lost during fruit development.[182] The ovary is usually 4-carpellate, although rarely it may have 3 or 6 carpels.[182] The carpels are antitepalous, each facing a tepal.[2][182] Their fused walls extend inwards as placentae, dividing the ovary into four incomplete locules.[2][182] The ovary has central placentae[49] and placentation is often described as lamellar[2] or laminar[182] (but see [194]). To these placentae are attached between 200 and 500 ovules.[2] The ovules are supplied by vascular connections running from the base of the carpel (and not by the "larger bundles in the dorsal carpel walls").[182] The ovules are erect and anatropous (inverted). As with most angiosperms, they are bitegmic, having two integuments. The ovules are crassinucellate, the megagametophyte being deeply seated within the nucellus.[2][182]

Beginning in the earliest stages of ovule development, the inner integument protrudes beyond the outer integument, the latter forming an apical, hooded structure; by the time of anthesis, the inner integument clearly extends beyond this hood.[182] The inner integument often becomes deflected on the placenta, with the micropyle (formed solely from the former) lying close the surface of the latter.[182] A prominent chalazal lobe and a small basal lobe form prior to anthesis, as the ovules assume their characteristic curvature (anatropy).[182] The funiculus is short and partly obscured by the integumentary hood in mature ovules.[182] In the vast majority of Nepenthes, the outer integument continues to lengthen on either side of the embryo following pollination, giving rise to the characteristic filiform wings of the seed[182] (although a number of species lack these appendages). In species with filiform seeds, the ovule grows to 15–25 times its length at anthesis over the course of its development,[182] a process that usually takes 6–8 weeks.[9] The inner integument turns papery as it forms the tegmen, the inner coat that surrounds the embryo.[182]

The stigmas are sessile, flat, and expanded,[4] and have a wet surface.[2] They number as many as the locules (usually 4),[2] each being partly subdivided into a pair of lobes.[182] The stigmas are almost smooth, particularly around their outer margins, and may be yellowish-green.[182] The gynoecium narrows slightly below the stigmas, forming a short style.[182] The upper stylar canal is large and funnel-shaped.[182]

Pollen[edit]

Mean pollen tetrad diameter of selected Bornean taxa[195]
Species MD     SE     CV (%) N           Species MD     SE     CV (%) N     
N. gracilis 27.0 0.3 6.6 120 N. veitchii 32.3 0.2 7.2 390
N. ampullaria 28.5 0.3 9.9 495 N. lowii 33.0 0.2 7.8 570
N. bicalcarata 28.9 0.4 7.5 120 N. reinwardtiana 33.6 0.2 7.0 780
N. hirsuta 28.9 0.4 7.9 120 N. × alisaputrana 33.7 0.6 9.0 110
N. mapuluensis 28.9 0.5 9.2 120 N. macrovulgaris 34.2 0.4 7.1 120
N. northiana 29.8 0.4 6.0 120 N. clipeata 34.4 0.4 6.6 120
N. tentaculata 29.8 0.4 9.4 210 N. edwardsiana 34.4 0.5 7.7 100
N. rafflesiana 30.5 0.4 10.9 345 N. rajah 34.7 0.3 7.0 300
N. mirabilis 31.0 0.6 9.8 120 N. fusca 34.8 0.6 9.1 120
N. albomarginata 31.8 0.4 6.2 120 N. mollis 37.2 0.4 6.1 120
N. muluensis 32.0 0.4 8.7 120 N. villosa 37.2 0.2 6.7 490
N. × hookeriana 32.2 0.3 7.6 120 N. ephippiata 38.5 0.3 3.8 120
N. faizaliana 32.3 0.4 7.6 120 N. × kinabaluensis 38.9 0.4 5.1 120
Measurements based on pollen samples taken from dried and pickled herbarium specimens.[195]

Nepenthes pollen appears to be relatively homogeneous with little variation observed between species.[195][196] The pollen grains are shed in tetrads (groups of four),[197] which are typically tetrahedral or, rarely, decussate[198] or isobilateral in N. ampullaria.[199] The tetrads bear spinules (spines) on their outer surfaces and are small- to medium-sized,[195] generally ranging in diameter from 24 to 35 µm (excluding the spinules) after acetolysis.[196] Specimens up to 40 µm have been reported by one author,[186] but it is uncertain whether the spines were included in this measurement.[2] Pollen development is normal.[182][200]

The dimensions of the pollen grains themselves are 17–25 by 16.5–23 µm.[2] Each grain consists of three cells when shed.[182] The grains lack apertures and are sub-elliptic to spheroidal in surface view.[2] Each has a single convex distal face (pointing outwards from the centre of the tetrad) and three flat proximal faces (pointing inwards), the latter being fused almost up to the equatorial plane.[2] The distal face appears smooth under an optical microscope, but scanning electron microscopy reveals its densely papillose surface covered in a lipid layer.[2] The pollen grains are strongly bound to eachother within the tetrads, resisting disintegration during acetolysis.[182] The tetrads also stick to each other slightly.[182] Dimorphism has been observed in the pollen of N. ampullaria, with 3.8% of the sampled grains lacking spinules but otherwise agreeing morphologically with the spinulose ones.[199]

Exine is the resistant outer wall of the pollen grains and is composed largely of sporopollenin. On its exposed distal surface, it is 1–1.5 µm thick and bears spinules. These are absent from the other surfaces, where the exine is considerably thinner.[2] The pointed spinules measure 0.5–3 µm in length by 0.5–1.5 µm in basal width, and are spaced 1–3.5 µm apart.[196] The exine is not stratified and lacks a columella.[201] A cellulose-rich cell wall, called intine, is present underneath the exine. Intine of adjacent pollen grains is connected via openings in the exine of the proximal walls (which itself exhibits some cohesion).[2]

Fossil pollen of various provenance, much of it originally described under the form taxon Droseridites, has been tentatively assigned to the genus Nepenthes by several authors. This includes pollen from Eocene formations in Europe (from France to the Caucasus; N. echinatus, N. echinosporus, and N. major),[202][203] from the Kerguelen Islands (originally described as D. spinosus),[202][203] and from the mid Miocene of northern Borneo.[204] If correctly identified, these specimens would represent the only known fossil record of the genus.[2] However, at more than 40 µm in diameter, the tetrads of D. major are larger than those of any known extant Nepenthes, and within the lower range of extant Drosera tetrads.[2] Some authors consider D. major and D. parvus to be synonyms of Nepenthidites laitryngewensis.[205][206]

Fruits[edit]

Left: Infructescence of N. pervillei

Centre: An infructescence of N. insignis from the island of Biak

Right: Opened seed capsules of N. tentaculata from Sulawesi

The inflorescence matures into an infructescence bearing non-fleshy fruits.[3] Fruit maturation varies in duration; in N. macfarlanei it takes around 6 months,[192] whereas research on selected Bornean species from Mount Kinabalu has produced a lower figure of 3 months for those taxa.[182][186][2] One study on N. macfarlanei found that approximately 60% of open pollinated female flowers mature into fruits and that each of these contains, on average, 92.5 fertile and 44.2 infertile seeds.[192][2]

The fruit is typically a grey to reddish brown[4] fusiform to ovate capsule;[2][4] N. pervillei is unique in that it has obconic fruits.[4] Ripe fruits are leathery or woody in texture and usually possess 4 valves, although N. pervillei is again atypical in that it has only 3 valves.[4] Fruits may be supported on a stipe.[2] Each fruit contains a large number of seeds, generally 100 to 500 per capsule,[49] although they can number as few as 50.[2]

Fruit capsules open loculicidally by longitudinal dehiscence; that is, the fruit splits through the ovary wall of each carpel, allowing the seeds to exit directly from the locules. This is preceded by the formation of sutures in the outer carpel walls.[182] As the capsule valves open only slightly, the seeds do not simply fall out but are removed over a period of time by successive gusts of wind; this is known as the 'censer' mechanism of seed dispersal, and is a type of anemochory.[2] (Nepenthes seeds lack structures such as elaiosomes, barbs, or hooks, which are typically adaptations for zoochory—dispersal by animals.)[2] Dried tepals may or may not persist at the base of the seed capsule.[4]

Seeds[edit]

With a few exceptions, the appearance of Nepenthes seeds is quite uniform throughout the genus.[207] The seeds are typically filiform, with the testa (seed coat) elongated into two hair-like appendages (also called wings) on opposite sides of the seed nucleus. They are silvery yellow to dark brown in colour[4] and measure 3[2]–35 mm, wings included[4] (the wingless seeds of N. pervillei are only 2–4 mm long).[4] The testa is reduced to an outer epidermis "with thick outer walls to the cells and irregular thickenings on the radial and inner walls".[2] The seed nucleus may be transversely and/or longitudinally wrinkled to varying degrees and may also bear prickles.[207] The latter may extend into adjacent areas of the seed appendages in species such as N. rafflesiana.[207][208] The tegmen (inner coat) is crushed and only produced around the embryonic cavity.[2] Endosperm is starchy and only present in very small quantities[4] or absent altogether;[2][182] the embryo is therefore readily identifiable and easily excised from the surrounding tegmen.[182] The embryo is very small and positioned centrally. It is straight or U-shaped and resides in a sub-ellipsoid cavity.[2] Both the unequal cotyledons and the hypocotyl are well developed, although very small.[2][182] Mature embryos reportedly lack a plumule (embryonic shoot apex).[182]

Although seeds are typically wind distributed, a number of species that grow in exposed, isolated sites show modified seed morphology to minimise dispersal by wind. The seed wings are greatly reduced in N. argentii, N. madagascariensis, N. masoalensis, N. northiana, N. sibuyanensis, and members of the Indochinese "N. thorelii aggregate"[44][45] (especially the island endemic N. kerrii[4][209]); they are altogether absent in N. pervillei.[4][167] The more cylindrical and robust seeds of these species prevent strong winds carrying them away from suitable habitats and allow for dispersal by water (hydrochory), particularly rainfall and small streams.[167] In addition, the shape of the seeds may allow them to more easily roll across rocks and find crevices where they may germinate, particularly in the case of N. pervillei plants growing on the island of Mahé.[4]

Roots[edit]

A plant of N. holdenii with its irregularly branched tubers exposed (left) and a closeup of the root system of the same specimen (right)

The roots of Nepenthes have been the subject of only limited research.[210] They are branched and fibrous, generally brown to black in colour, and usually less than 2 mm in diameter.[1][4] Epiphytic species often have poorly developed root systems and some appear to lack them altogether, existing only as climbing stems.[1] Plants that grow terrestrially produce more extensive root systems,[1] though these are often shallow.[4] The roots of plants growing on entirely inorganic substrates serve mainly to absorb water and to anchor the plant.[4] In large specimens of some species, such as N. veitchii, the oldest parts of the stem may die away and roots may grow down from nodes on the stem.[9] Such adventitious roots may also be seen in stems that have been broken or otherwise damaged. A good example of this is N. chaniana; the long, fragile stems of this species break quite often, with the apical portion subsequently establishing itself as a new plant.[12][211][80]

Fresh annual growths of fine fibrous roots are yellowish-green at the apex, but quickly turn black-brown. They bear numerous brown root hairs, which remain functional throughout the season. Although root development in Nepenthes has occasionally been described as weak, the root system is often well developed; annual development produces a greatly branched root system. Over time, a root cambium forms together with associated tissues, resulting in the brown epidermis and underlying cortex splitting and eventually being shed. These exposed tissues subsequently assume a yellow or flesh colour that may be retained for years, before finally turning yellow-brown.[9]

The rootstock of a N. mirabilis plant from New Guinea

Tubers and rhizomes[edit]

Species that experience a dry season often have a well developed, tuberous rootstock, which aids in water and food storage and allows them to survive low intensity bushfires.[33][11][4] This is particularly common among the pyrophytic Nepenthes of Indochina,[212] which form the so-called "N. thorelii aggregate" that includes[44] N. andamana,[191] N. bokorensis,[39] N. chang,[184] N. holdenii,[44] N. kampotiana,[4] N. kerrii,[209] N. smilesii,[4] N. suratensis,[213] and N. thorelii,[45][214] as well as the undescribed N. kongkandana.[4] This tuberous root system is also found in at least some populations of N. mirabilis var. globosa[6] and may also be present in other Thai populations of N. mirabilis.[4]

These species undergo a form of dormancy during periods of severe drought.[4] A similar enlargement of the root system is seen in N. rowanae of Australia,[33] but the adaptation is believed to have evolved independently in this species.[4] The rootstock is often carrot-shaped and may be irregularly branched.[4] Some of the roots themselves may also be swollen, but it is unknown whether these are used for storage in the same way.[4]

Some species, such as N. ampullaria and N. rhombicaulis, produce extended underground rhizomes.[1] Nepenthes argentii is noted for its long, vertical rhizome.[2]

Field observations and experiments with cultivated plants suggest that Nepenthes form mycorrhizal associations with fungi.[1][4][215][216]

Indumentum[edit]

Left: A densely hirsute pitcher bud of N. chaniana. Developing parts are often more hairy than mature ones, having caducous hairs that are lost with age.
Centre: A developing pitcher of a particularly hairy variant of N. hamata with a shaggy, fur-like indumentum. This trap was produced by a cultivated plant grown from wild collected seeds.
Right: Various epidermal hairs of Nepenthes, from an illustration in J. M. Macfarlane's 1908 monograph, "Nepenthaceae".[9] A1: surface view of brown peltate hair, A2: side view of brown peltate hair, B: brown rosette hair, C: brown branched hair, D: elongated brown hair, E: clear, thin-walled stellate hair of N. veitchii, F: hair of N. burkei, G & H: hairs of N. madagascariensis.[9]

Most species have some form of indumentum (covering of hair). These hairs, or non-glandular trichomes,[2] vary widely in form and colour, and can be diagnostic in some species. In an exhaustive 1971 study,[217] Rudolf Schmid-Höllinger identified five main types of multicellular Nepenthes hairs: simple hairs, tufted hairs, rosette hairs, arachnoid hairs, and hairs with teeth. Other authors have referred to tufted hairs as branched or dendritic,[2][218] while rosette hairs have also been called stellate.[2] Bifid and fasciculate hairs have also been recorded.[2]

Tufted hairs, in their various forms, are the the most common type.[2] Of these, one of the most frequently encountered consists of a single large branch with numerous smaller branches concentrated around its base, giving it the appearance of an unbranched hair under lower magnifications.[2] Simple, unicellular hairs are apparently rare.[2][218]

Developing parts are often densely hirsute, possibly to protect them against herbivory[66] or to collect moisture.[4] These hairs are often caducous, being shed during the course of development. Even species whose mature pitchers are completely glabrous (lacking hairs), such as N. flava and N. inermis, often have densely hirsute developing tendril buds.[4] Mature parts that usually bear an indumentum include the inflorescence, outer surfaces of the pitcher cup and lid, the tendrils, the stem, and the underside of the lamina.[2] Lower pitchers are often more densely hairy than upper pitchers and it has been proposed that these hairs help insects reach the pitcher mouth.[4] In some plants, a light-coloured indumentum may aid in cooling. In podsol Sundaland heath forest, white sands may become very hot in exposed sites. A white variant of N. rafflesiana (sometimes called N. rafflesiana var. nivea) is common in this habitat. It is believed that its light-coloured stem hairs may be an adaptation to maximise the reflectance of the harsh sunlight.[66] A glabrous variety (sometimes called N. rafflesiana var. glaberrima) is found in more shaded areas.[27]

Hairs are never present on the inner surface of the pitcher cup, which is one feature that distinguishes Nepenthes from the New World pitcher plants of the family Sarraceniaceae.[4] They are also absent from the peristome and rarely present on the upper surface of the lamina and underside of the lid; N. hurrelliana, which has one of the most conspicuous indumentums of any Nepenthes species, is noted for bearing hairs on the upper surface of the lamina, the base and margins of the lower lid surface, and even on the glandular crest and apical appendage of the lid.[66] Certain forms of N. hamata have extremely long, dense, and shaggy hair covering their pitchers and parts of the inflorescence.[4] At the other extreme, N. ceciliae lacks hairs on both vegetative and floral parts.[219][67] In other species, such as N. glabrata, the indumentum may be so highly reduced and localised as to appear completely absent.[2]

A lower pitcher with an intact band of trichomes (left) and one lacking them (right)

Those of N. albomarginata form a conspicuous band below the peristome, which apparently attracts termites to the pitcher mouth.[220] This band is up to 5 mm wide and is always white in freshly opened pitchers, but may turn orange or brown with age.[4] It is retained in at least some natural hybrids involving N. albomarginata, such as N. × cincta.REF A tomentose band under the peristome has occasionally also been observed in other species, including certain populations of N. mirabilis, although it is never as prominent as in N. albomarginata.[4] Nepenthes khasiana may have a somewhat similar orange to red band extending for several millimetres under the peristome, but this is non-hairy.[4]

Notes[edit]

a.^ The N. gymnamphora group of related taxa has been variously interpreted as comprising a single extremely variable species (N. gymnamphora);[1][221] two distinct species, one from Java (N. gymnamphora) and one from Sumatra (N. pectinata);[11] or two species, one with a wide distribution covering Java and Sumatra (N. gymnamphora) and one with a very restricted range in Sumatra (N. xiphioides).[144] An additional fourth undescribed taxon that resembles N. gymnamphora is known from Mount Sorik Merapi in Sumatra.[1] Following Charles Clarke's 2001 monograph,[1] all four taxa are treated under N. gymnamphora here.

a.^ In a 1996 issue of the Carnivorous Plant Newsletter, David Wong writes that "N. ampullaria grow to tremendous heights, it is not uncommon to see vines climbing up to more than a couple hundred feet [60 m] tall".[90] However, no major monograph on the genus mentions such a height; the greatest maximum height given for this species is "20 m or more".[4]

a.^ Cultivated plants have been known to sometimes produce 'doubled' pitchers, consisting of a pair of fused pitcher cups with separate lids.[222] Similar deformities have been seen in other carnivorous plant genera.[223]

b.^ Some authors treat N. fallax in synonymy with N. stenophylla,[11][12] while others consider them to be two distinct species, with plants commonly referred to as N. stenophylla actually representing N. fallax.[221] As in Matthew Jebb and Martin Cheek's 1997 monograph[11] and Charles Clarke's 1997 monograph,[12] the first interpretation is followed here.

d.^ In most cases, the inflorescence rises high above surrounding vegetation such that it is exposed to air currents for efficient seed dispersal.[186][192] However, in some species, such as N. northiana and N. tentaculata, the inflorescence may be produced under a sparse tree canopy.[2]

Aberrant floral growth in a specimen of the manmade hybrid N. alata × N. spathulata, consisting of a single giant flower with numerous crowded tepals and anthers. The image on the left shows the developing flower; the one on the right shows the freshly opened bloom 5 days later.

d.^ Cultivated Nepenthes plants have on occasion been observed to produce inflorescences consisting of a single very large flower with more than a dozen tepals. This aberrant growth seems to occur most commonly in young plants that are flowering for the first time. One such record is of a cultivated male N. rafflesiana.[224] The flower of this specimen produced pollen, although its viability was not determined. Subsequent male inflorescences produced by the same plant were normal.[224] Similar examples of abnormal floral growth have been recorded in other Nepenthes taxa.[225]

Perfectly "doubled" flowers have also been recorded.[226][227]

e.^ In Pitcher Plants of the Old World, Stewart McPherson writes:[4]

All Nepenthes inflorescences take the form of a panicle. [...] The more advanced species have only simple lateral axes, and very closely resemble true racemes; these inflorescences are not in fact racemes, but racemic panicles, though they are often referred to as racemes for the sake of simplicity or as a result of misinterpretation.

e.^ There is one record of an apparently hermaphroditic inflorescence produced by a cultivated N. mirabilis.[228] In another case, Julius August Lörzing claimed that a N. spectabilis plant he had collected (Lörzing 8297) bore a monoecious inflorescence. However, in his review of the genus, B. H. Danser could not find a specimen at the designated herbarium that matched this description and "call[ed] this record into question".[229] Summarising, Danser wrote that "[d]ata concerning monoeceous [sic] plants are very rare and not beyond doubt".[10]

f.^ Many authors consider N. hispida to be a variety of N. hirsuta,[38] while others believe it can be reliably distinguished on the basis of some vegetative features.[11][12][66] As in Matthew Jebb and Martin Cheek's 1997 monograph[11] and Charles Clarke's 1997 monograph,[12] the second interpretation is followed here.

g.^ Some authors choose to distinguish N. carunculata as a distinct species,[129] while others consider it to be a synonym of N. bongso.[11][1] As in Matthew Jebb and Martin Cheek's 1997 monograph[11] and Charles Clarke's 2001 monograph,[1] the latter interpretation is followed here.

h.^ In this study N. inermis was misidentified as N. bongso.[1]

i.^ N. thorelii is a poorly known Indochinese species with a confused horticultural history. The name has been widely applied to cultivated plants, but it is not certain whether the species exists in cultivation at all. Numerous artificial hybrids long-thought to involve N. thorelii may actually represent crosses with other species (or even crosses between different forms of the same species).[230]

References[edit]

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Further reading[edit]

  • Mullins, J. & M.H.P. Jebb 2009. Phylogeny and biogeography of the genus Nepenthes. National Botanic Gardens, Glasnevin.
  • Hernawati & P. Akhriadi 2006. A Field Guide to the Nepenthes of Sumatra. PILI-NGO Movement, Bogor.
  • Kubitzki, K. 2003. Nepenthaceae. In: K. Kubitzki & C. Bayer The Families and Genera of Vascular Plants. Volume V: Malvales, Capparales and Non-betalain Caryophyllales. Springer-Verlag, Berlin. pp. 320–324.
  • van Balgooy, M.M.J. 2001. Nepenthaceae. In: Malesian Seed Plants: portraits of non-tree families, Volume 3. Nationaal Herbarium Nederland, Leiden.
  • Naoki, T. 1999. Investigation of tropical alpine plant Nepenthes in Peninsular Malaysia. 2. Journal of Insectivorous Plant Society (Japan) 50(3): 77–82.
  • Beaver, R.A. 1979. Biological studies of the fauna of pitcher plants (Nepenthes) in West Malaysia. Annales de la Société Entomologique de France 15(1): 3–17.
  • Beaver, R.A. 1983. The communities living in Nepenthes pitcher plants: fauna and food webs. In: J.H. Frank & L.P. Lounibos (eds.) Phytotelmata: Plants as Hosts for Aquatic Insect Communities. Plexus Publishing, New Jersey. pp. 129–159.
  • Beaver, R.A. 1985. Geographical variation in food web structure in Nepenthes pitcher plants. Ecological Entomology 10(3): 241–248. doi:10.1111/j.1365-2311.1985.tb00720.x
  • Beccari, O. 1886. Rivista delle specie del genere Nepenthes. Malesia 3: 1–15.
  • Danser, B.H. 1927. Indische bekerplanten. De Tropische Natuur 16: 197–205.
  • Fish, D. & R.A. Beaver 1979. A bibliography of the aquatic fauna inhabiting bromeliads (Bromeliaceae) and pitcher plants (Nepenthaceae and Sarraceniaceae). Proceedings of the Florida Anti-Mosquito Association (19th meeting, April 1978) 49: 11–19.
  • Henderson, M.R. 1974. Nepenthaceae. In: Malayan Wild Flowers: Dicotyledons. The Malayan Nature Society, Kuala Lumpur.
  • Moran, J.A. 1993. Pitcher allocation strategy of the pitcher plant Nepenthes rafflesiana. Brunei Museum Journal 8: 77–80.
  • Miquel, F.A.G. 1870. Nepenthes. Illustrations de la flore l'Archipel Indien 1: 1–48.
  • Osunkoya, O.O., S.D. Daud, B. Di Giusto, F.L. Wimmer & T.M. Holige 2007. Construction Costs and Physico-chemical Properties of the Assimilatory Organs of Nepenthes Species in Northern Borneo. Annals of Botany 99(5): 895–906. doi:10.1093/aob/mcm023
  • Ridley, H.N. 1967. Nepenthaceae. In: The Flora of the Malay Peninsula. L. Reeve & Co., London.
  • Shivas, R.G. 1984. Pitcher plants of Peninsular Malaysia and Singapore. Maruzen Asia, Kuala Lumpur.
  • Veitch, H.J. [1906] 1979. "An Abridged History of Nepenthes." (PDF).  Carnivorous Plant Newsletter 8(1): 20–23.
  • Wallace, A.R. 1869. The Malay Archipelago, Volume I. Macmillan, London.
  • Adam, J.H. 1990. Taxonomic and Ecological Studies of Bornean Nepenthes. Ph.D thesis, University of Aberdeen, Scotland.
  • Adam, J.H. 1995. The diversity, ecology and conservation of Nepenthes (Nepenthaceae) in Sabah State of Malaysia. In: The 4th ASEAN Science and Technology Week. pp. 29–48.
  • Adam, J.H. 2002. Population structure of Nepenthes species (pitcher plants) from Weston, Sipitang in Sabah. Proceedings of the 4th International Carnivorous Plant Conference, Tokyo, Japan. pp. 15-21.
  • Adam, J.H. 2002. Ecology and Diversity of Pitcher Plants in Sarawak. Proceedings of the 4th International Carnivorous Plant Conference, Tokyo, Japan. pp. 165–169.
  • Adam, J.H. 2002. Population structure of Nepenthes from adjacent area of Taman Tun Fuad Stephen in Kota Kinabalu, Sabah. The Sarawak Museum Journal 57(78): 283–298.
  • Adam, J.H. & C.C. Wilcock 1998 ['1996']. Pitcher plants of Mt. Kinabalu in Sabah. The Sarawak Museum Journal 50(71): 145–171.
  • Adam, J.H., C.C. Wilcock & M.D. Swaine 1992. The ecology and distribution of Bornean Nepenthes. Journal of Tropical Forest Science 5(1): 13–25.
  • Alex-Kong, S.P. 2002. Study on Community Structure of Pitcher Plants (Nepenthes) in Selected Area in Sibu, Sarawak. B.Sc. thesis, Universiti Kebangsaan Malaysia.
  • Daiman, D. 2002. A Study on the Community Structure of Nepenthes in Natural Forest Education Park, Universiti Kebangsaan Malaysia Bangi. B.Sc. thesis, Universiti Kebangsaan Malaysia.
  • Heslop-Harrison, Y. 1975. Enzyme release in carnivorous plants. Frontiers in Biology 43(4): 525–578. PMID 780147
  • Holttum, R.E. 1940. Malayan pitcher plants. Malayan Nature Journal 1: 35–44.
  • Lee, C.C. 2002. Nepenthes species of the Hose Mountains in Sarawak, Borneo. Proceedings of the 4th International Carnivorous Plant Conference, Hiroshima University, Tokyo: 25–30.
  • Talib, M.R. 2004. A Study on the Community Structure of Nepenthes in Lowland Area of Bandar Baru Behrang, Perak Darul Ridzuan. B.Sc. thesis, Universiti Kebangsaan Malaysia.
  • Albert, V.A. & D.W. Stevenson 1996. Morphological cladistics of the Nepenthales. American Journal of Botany 83(6, supplement): 135.
  • Kajii, E., T. Kamesaki, S. Ikemoto & Y. Miura 1988. Decomposing enzymes against human blood-group antigens in the extract of Nepenthes alata. Die Naturwissenschaften 75(5): 258–259. PMID 3405311
  • Kajii, E., T. Kamesaki & S. Ikemoto 1991. The effect of the Nepenthes alata extract on the cold agglutinin-associated antigens. Nihon Hōigaku Zasshi 45(1): 30–32. PMID 2046171
  • Kamesaki, T., E. Kajii & S. Ikemoto 1989. Purification of the decomposing enzyme from Nepenthes alata against glycophorin B of human red blood cells by high-performance liquid chromatography. Journal of Chromatography 489(2): 384–389. PMID 2666423
  • Oye, P.v. 1921. Zur Biologie der kanne von Nepenthes melamphora Reinw.. Biologisches Zentralblatt 41: 529–534.
  • Reuter, L. 1938. Protoplasmatik der Stomata-Zellen der Gleitzone der Nepenthes-Kanne. Protoplasma 30(1): 273–282. doi:10.1007/BF01613754
  • Roth, I. 1953. Zur Entwicklungsgeschichte und Histogenese der Schlauchblätter von Nepenthes. Planta 42(3): 177–208 doi:10.1007/BF01938569
  • Roth, I. 1954. "Entwicklung und Histogenetischer Vergleich der Nektar- und Ver-dauungsdrüsen von Nepenthes." (PDF).  Planta 43(5): 361–378. doi:10.1007/BF01914911
  • Santo, M.J., J.S. Massa, & T.P. Owen 1998. Glandular secretion and absorption in the carnivorous pitcher plant Nepenthes alata. American Journal of Botany 85(supplement): 92.
  • Lüttge, U. 1964. Untersuchungen zur Physiologie der Carnivoren-Drüsen. III. Der Stoffwechsel der resorbierten Substanzen. Flora 155: 228–236.
  • Lösch, R. Kannenpflanzen: Insektenfressende Standortspezialisten und biogeographische Indikatoren. Biologie in unserer Zeit 20(1): 26–32. doi:10.1002/biuz.19900200111
  • Russell, C. & E. Ossian 1990. Opportunistic feeding involving the pitcher plants Nepenthes hirsuta, Nepenthes gracilis and the epiphytic orchid Schomburgkia tibicinis, or natural ant eradication, the rube goldberg method. The Orchid Digest 54(4): 182–184.
  • Kandler, O., & H. Schmideder 1952. Untersuchungen über die Geschwindigkeit der Fibrinverdauung bei Nepenthes. Zeitschrift für Botanik 40: 317–326.
  • Clautriau, G. 1900. La digestion dans les urnes de Nepenthes. Mém. Couronnés et autres Mém. Acad. roy. Belg. Cl. Sci. 59: 1–55.
  • Vines, S.H. 1898. The proteolytic enzyme of Nepenthes. II. Annals of Botany 12: 545–555.
  • de Meijere, J.C.H. 1910. Nepenthes-Tiere I. Systematik. Annales du Jardin Botanique de Buitenzorg 3(supplement): 917–940.
  • Stern, K. 1917. Contribution to the knowledge of Nepenthes. Flora 109: 213–283.
  • Anderson, A.N. 1994. Secretion and absorption in glands of the carnivorous plant Nepenthes alata. B.A. (Hons.) thesis, Connecticut College, New London.
  • Lennon, K.A. 1995. A study of the structural and functional adaptations of the pitcher plant Nepenthes alata to its carnivorous habit. B.A. (Hons.) thesis, Connecticut College, New London.
  • Bauer, U., C. Willmes & W. Federle 2009. Effect of pitcher age on trapping efficiency and natural prey capture in carnivorous Nepenthes rafflesiana plants. Annals of Botany 103(8): 1219–1226. doi:10.1093/aob/mcp065
  • Harrison, J.F. 2001. Insect acid–base physiology. Annual Review of Entomology 46: 221–250. doi:10.1146/annurev.ento.46.1.221
  • Hooker, J.D. Address to the Department of Zoology and Botany. Report to the British Association for the Advancement of Science: Report of the Forty-Fourth Meeting, Belfast (1875) 1874:102–116. FIX REF
  • Juniper, B.E. & J. Burras 1962. How pitcher plants trap insects. New Scientist 13: 75–77.
  • Pavlovič, A., L. Singerová, V. Demko & J. Hudák 2009. Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis. Annals of Botany 104(2): 307–314. doi:10.1093/aob/mcp121
  • Takahashi, K., S.B.P. Athauda, K. Matsumoto, S. Rajapakshe, M. Kuribayashi, M. Kojima, N. Kubomura-Yoshida, A. Iwamatsu, C. Shibata & H. Inoue 2005. Nepenthesin, a unique member of a novel subfamily of aspartic proteinases: enzymatic and structural characteristics. Current Protein and Peptide Science 6(6): 513–525. doi:10.2174/138920305774933259