| Nepenthes bicalcarata | |
|---|---|
 | |
| Intermediate pitcher ofN. bicalcarata | |
Scientific classification | |
| Kingdom: | Plantae |
| Clade: | Tracheophytes |
| Clade: | Angiosperms |
| Clade: | Eudicots |
| Order: | Caryophyllales |
| Family: | Nepenthaceae |
| Genus: | Nepenthes |
| Species: | N. bicalcarata |
| Binomial name | |
| Nepenthes bicalcarata | |
| Synonyms | |
Nepenthes bicalcarata (/nɪˈpɛnθiːzbaɪˌkælkəˈrɑːtə,-bɪˌkælkəˈreɪtə/; fromLatin for "two-spurred"), also known as thefanged pitcher-plant,[4] is a tropicalpitcher plant which isendemic toBorneo. It is avine up to 40 m (130 ft) length. It is amyrmecophyte noted for itsmutualistic association with a species ofant,Camponotus schmitzi. As anant-fed plant it lacks many of the features that characterise the carnivorous syndrome inNepenthes, includingviscoelastic and highly acidic pitcher fluid, the waxy zone of the pitcher interior, and possibly even functionaldigestive enzymes.[5]
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Nepenthes bicalcarata wasformally described byJoseph Dalton Hooker in his 1873 monograph, "Nepenthaceae", based on specimens collected byHugh Low andOdoardo Beccari near theLawas River in Borneo.[2] Thetype specimen,Low s.n., is deposited at theRoyal Botanic Gardens, Kew.[6] Seven years later,Spencer Le Marchant Moore describedNepenthes dyak, based on a specimen (Teijsmann 10962) collected byJohannes Elias Teijsmann fromKapuas River nearSintang in western Borneo.[3][7] This specimen is also held at the Royal Botanic Gardens, Kew[6] and a duplicate is deposited at theNational Herbarium of the Netherlands inLeiden.[8]Nepenthes dyak was later mentioned several more times in the botanical literature,[9][10] but is now considered conspecific withN. bicalcarta.[11]
Nepenthes bicalcarata was introduced to Europe in 1879 by British explorerFrederick William Burbidge, who collected plants for the famousVeitch Nursery. These were cultivated to larger size and distributed in 1881.[4]
During this time, interest inNepenthes had reached its peak. A note inThe Gardeners' Chronicle of 1881 mentions the Veitch Nursery'sN. bicalcarata as follows:[12]
"Then there isN. bicalcarata, a most robust habited kind with sturdy foliage and bag-like pitchers provided with a vicious-looking rat-trap-like apparatus in its lid which renders it very distinct from its neighbours."
Several years after its introduction,N. bicalcarata was still very much a horticultural rarity. In Veitch's catalogue for 1889,N. bicalcarata was priced at£3.3s per plant, while the famous giant-pitcheredN. northiana andN. rajah were selling for £2.2s.[4]
Nepenthes bicalcarata plants are the largest in the genus, climbing up to 20 m into the forestcanopy. The cylindrical stem is thicker than that of any otherNepenthes species, measuring up to 3.5 cm in diameter.Internodes are up to 40 cm long.[11][13]
The leaves ofN. bicalcarata arepetiolate andcoriaceous in texture. Thelamina isobovate-lanceolate in form and also reaches huge dimensions, growing to 80 cm in length and 12 cm in width.[14] It is slightlydecurrent on the stem, forming two narrow wings. The lamina has indistinct longitudinal veins and numerouspennate veins. Thetendrils may be up to 60 cm long and 8 mm wide. They are hollow and swollen near the pitcher,[11] and are the primary residence of the ants. The ants get much of their food from numerous, largeextrafloral nectaries.
Although most parts of the plant are very large, the pitchers themselves do not rival those of species such asN. rajah. Nevertheless, they may have a volume of over one litre and grow up to 25 cm high and 16 cm wide. A pair of prominent fringed wings (≤15 mm wide) runs down the front of lower pitchers. These are usually reduced to ribs in aerial pitchers. Theperistome (≤20 mm wide) is characteristically flattened and curved inwards.[11] The inner portion of the peristome accounts for around 70% of its total cross-sectional surface length.[15] It bears small but distinct teeth. The two sharp spines for which the species is famous are present on the underside of the pitcher lid, and may be 3 cm long. They are derived from the uppermost 10–12 peristome ribs.[16] The pitcher lid oroperculum isreniform tocordate and has no appendages. An unbranchedspur (≤15 mm long) is inserted at the base of the lid.[11]
Nepenthes bicalcarata has apaniculateinflorescence. Thepeduncle may be up to 40 cm long and therachis can reach 100 cm in length. Female inflorescences are usually shorter.[17] Branches on the flower stem are up to 40 mm long and bear up to 15 flowers.Sepals are eitherobovate orlanceolate and up to 4 mm long.[11] A study of 120pollen samples taken from a herbarium specimen (Fosberg 43860, altitude not recorded) found the mean pollen diameter to be 28.9μm (SE = 0.4;CV = 7.5%).[18]
Mature plants are virtuallyglabrous.Caducous hairs are present on the youngest parts of the plant and on the inflorescences.
Nepenthes bicalcarata varies little across its range. Consequently, noinfraspecific taxa have been described.[11]
Nepenthes bicalcarata isendemic toBorneo. It is most common in thepeat swamp forests of the western coast of the island, which stretch acrossSarawak,Sabah,Kalimantan, andBrunei. There it often grows in the shade of the ubiquitousdipterocarpShorea albida.[4]Nepenthes bicalcarata also occurs inkerangas forest and has even been recorded from white sandheath forests in Sarawak andEast Kalimantan.[4] The species is oftensympatric withN. ampullaria in these habitats.[11]
Specimens growing in undisturbed peat swamp forest, where sunlight is greatly diffused and high humidity prevails, reach the largest dimensions.[11]Nepenthes bicalcarata has a shallow root system that only penetrates the top layer ofpeat andleaf litter, to a depth of about 25 cm. Below this, high concentrations oftannins andalkaloids render the substrate toxic.[4]
Nepenthes bicalcarata is generally found below 300 m in altitude, althoughJohannes Gottfried Hallier reported a single collection in 1894 from between 700 and 950 m above sea level.[19]
Theconservation status ofN. bicalcarata is listed asVulnerable on the2006 IUCN Red List of Threatened Species based on an assessment carried out in 2000.[1] In 1997,Charles Clarke informally classified the species asNear Threatened based on theIUCN criteria.[11] This agrees with the conservation status assigned toN. bicalcarata by theWorld Conservation Monitoring Centre.[20]
The two thorns that giveN. bicalcarata its name are unique to this species and bear some of the largestnectaries in the plant kingdom.[21][22][23] The purpose of these structures has long been debated among botanists.Frederick William Burbidge suggested that they might serve to deterarborealmammals such astarsiers,lorises andmonkeys from stealing the contents of the pitchers.[11][24] In an article published in 1982, Cliff Dodd speculated on the function of the thorns, but did not believe they play a role in prey capture.[25]Charles Clarke observed that monkeys and tarsiers rip the pitchers open at the sides in order to feed from them, rather than reaching in through the pitcher mouth.[26] However, he found that the mammals attacked the pitchers ofN. bicalcarata less frequently than those of other species, such asN. rafflesiana.[26] Clarke's observations suggest that the spines likely serve to lure insects into a precarious position over the pitcher mouth, where they may lose their footing and fall into the pitcher fluid, eventually drowning.[26] A similar trapping method is employed by theSumatran endemicN. lingulata, which has a singlefiliform appendage positioned over the pitcher mouth. However, in that species the appendage is a structure of the lid and not the peristome.[27]
Together withN. ampullaria andN. ventricosa,N. bicalcarata is unusual in that the glandular region of the pitcher extends almost to the peristome, such that there is little or no conductive waxy zone.[15][28][29][30] The waxy zone functions by causing prey to slip and fall into the digestive fluid. A 2004 study found that the peristome ofN. bicalcarata plays a very important role in prey capture. When it is dry, the peristome is highly ineffective in catching insect prey, but when wetted, the capture rate increases more than three-fold.[28]
A 1999 study of pitcher morphology and spectral reflectance characteristics showed thatN. bicalcarata has no colour contrast maximum between the peristome and pitcher cup in theultraviolet waveband, but small maxima of –0.17 at 450 nm (violet), 0.32 at 548 nm (green), and –0.16 at 668 nm (red).[31] This means that the peristome is less reflective than the pitcher cup in the violet and red bands, but more reflective in the green band. The contrast maxima in the green and blue regions seem to correspond to insect visual sensitivity maxima, while the others do not.[31] Based on their findings, the authors made the "tentative prediction" that the upper pitchers ofN. bicalcarata are less successful at catching anthophilous (flower-visiting) prey than those of sympatricN. rafflesiana.[31]
Nepenthes bicalcarata plays host to an unusual species ofant that makes its nest in the plant's hollow tendrils.[11][32][33][34] Described asCamponotus schmitzi in 1933,[35] it is a member of the extremely populous and widespread genus ofcarpenter ants.
This unique animal–plant interaction was noted byFrederick William Burbidge as early as 1880.[36] In 1904,Odoardo Beccari suggested that the ants feed on insects found on and around the plant, but may fall prey to it themselves.[37] In 1990, B. Hölldobler andE. O. Wilson proposed thatN. bicalcarata andC. schmitzi form amutually beneficial association.[38] At the time, however, no experimental data existed to support such a hypothesis. A series of observations and experiments carried out inBrunei byCharles Clarke (published in 1992 and 1998),[39][40][41] and by Clarke and Roger Kitching (1993 and 1995),[42][43] strongly support themutualism theory.
Nepenthes bicalcarata is amyrmecotroph (ant-fed plant), obtaining nutrients fromC. schmitzi in the form ofegesta and, occasionally, ant remains. It has been estimated that this input accounts for 42% of the plant's total foliarnitrogen (76% in plants with ant occupancy rates above 75%).[5] The ants increase nutrient retention in the pitchers by preying oninfaunal flies, which would otherwise eventually leave their hosts and thereby act askleptoparasites. This nutrients later becomes available to the plant through the ants' waste.[44]Camponotus schmitzi has also been observed to attack newly caught insects and therefore prevent prey escape.[45][46] At other times, the ants are very passive, remaining hidden under the inner peristome fold, presumably so as not to dissuade visitation by potential prey species.[45] This behaviour is in stark contrast to othermyrmecophytic ants, which are typically highly territorial.[45] John Thompson has suggested thatN. bicalcarata may be the only plant species that obtains nutrients through both insect capture and ant-hosting habits.[47]
Camponotus schmitzi is able to swim in the pitcher fluid using tripod-like leg coordination similar to that of terrestrial locomotion[48][49] and can remain submerged for up to 30 seconds.[50] When feeding, it appears to target large prey items only, cooperatively retrieving them from the fluid.[50] Hauling food from the pitcher fluid to the peristome—a distance of no more than 5 cm—may take up to 12 hours.[11] In this way the contents ofN. bicalcarata pitchers is controlled such that organic matter does not accumulate to the point ofputrefaction, which could lead to the demise ofpitcher infauna (which may also benefit the plant) and sometimes the pitcher itself.[11][51]
The ants have been observed to clean the peristome of fungalhyphae and other contaminants, thereby maintaining high trapping efficiency over the pitcher's lifespan.[52][53] Research conducted by Dennis and Marlis Merbach has shown thatC. schmitzi also benefitsN. bicalcarata by protecting it from pitcher-destroyingweevils of the genusAlcidodes.[54][55] In order to create a favourable environment for its pitcher inhabitants, it appears thatN. bicalcarata actively maintains thepH of its pitcher fluid at a less acidic level than that found in most otherNepenthes species[29][45] (this might explain the occasional presence oftree frog eggs in its pitchers).[29] In doing so, however, the plant reduces its ability to digest and assimilate nutrients from captured prey. The pitcher fluid ofN. bicalcarata is also lessviscoelastic than that of mostNepenthes species, and appears to lack functionaldigestive enzymes.[5]Nepenthes bicalcarata is therefore highly reliant on its ant symbiont. Indeed, plants not inhabited byC. schmitzi do not appear to benefit significantly from carnivory, with any gains from prey digestion being offset by the high costs of pitcher construction.[5] Conversely, ant-inhabited plants have more leaves and a greater total leaf area, and ant presence is associated with lower pitcher abortion rates and more voluminous pitchers (and consequently greater preybiomass).[5][56][57] Studies have shown that plants colonised byC. schmitzi have more nitrogen available to them, and a higher proportion of it is insect-derived.[44]
Camponotus schmitzi nests solely in the tendrils ofN. bicalcarata and rarely ventures onto other plants. The species is completely dependent onN. bicalcarata for food anddomicile.[11]Nepenthes bicalcarata, on the other hand, is able to survive and reproduce without the presence of the ants; it is afacultative mutualist. This being the case, there appear to be few mature plants over 2 metres in height not colonised byC. schmitzi.[11] The ants seem to favour upper pitchers and rarely colonise lower pitchers.[58] This is likely due to the fact that terrestrial traps are periodically submerged in water during heavy rains. Flooding of the ants' nest chamber could result in the demise of the ant colony, particularly the developing eggs,larvae, andpupae.[23]
A species ofmite,Naiadacarus nepenthicola, appears to be restricted to the pitchers ofN. bicalcarata. It is thought to feed on decomposing leaves and insects that are caught in the pitchers.Deutonymphs of this mite are dispersed throughphoresy onC. schmitzi.[59]
_of_samples_and_assessment_of_myrmecotrophy.png)
Left centre: Effect ofC. schmitzi occupancy on leaf apex abortion and pitcher production rates. In the first chart (A), cases where the tendril was found to be cut are grouped under unknown fate (denoted with a question mark) and "pitcher" encompasses both living and dead traps (in non-pitchering plants, the latter).[5]
Right centre: Prey biomass accumulated over a pitcher's entire lifespan as a function of pitcher volume in ant-occupied and unoccupied lower pitchers.[5]
The following naturalhybrids involvingN. bicalcarata have been recorded.
None of these hybrids are known to be colonised byC. schmitzi as is the parent speciesN. bicalcarata.[11]
SinceN. ampullaria andN. bicalcarata are often sympatric in the wild, it is not surprising that they occasionally hybridise. Several examples of this natural hybrid are known fromBrunei, where it grows inpeat swamp forest andheath forest.[11] It was first recorded byMitsuru Hotta in 1966.[61]
Pitchers bear the characteristic thorns ofN. bicalcarata, although they are greatly reduced in size. The mouth is round and the lid isovate-cordate in form. This hybrid resemblesN. × hookeriana to a certain extent, but differs in having spines on the underside of the lid and more globose upper pitchers with a smaller lid.[11]
Aerial pitchers ofN. ampullaria ×N. bicalcarata are usually dominated by characteristics ofN. ampullaria. They are often very small and unable to function in a normal manner.[11]
This rare complex hybrid was discovered in the lowland forests ofBrunei. It produces small speckled pitchers with reduced thorns under the lid. The plant is intermediate in appearance betweenN. × trichocarpa andN. bicalcarata.
This hybrid has been namedN. × cantleyi afterRob Cantley. The morphology of the pitchers closely resemblesN. bicalcarata, although the peristome is more similar to that ofN. gracilis. The characteristic spines ofN. bicalcarata are greatly reduced and are only present as small bumps. This hybrid has the growth habit ofN. gracilis, with the stem scrambling along the ground. It grows in open, sandy areas. The pitcher fluid is notablyacidic like that ofN. gracilis, withpH values as low as 1.82 being recorded.[11]
This natural hybrid is rare and is only known from Brunei, where it involvesN. mirabilis var.echinostoma. It closely resemblesN. bicalcarata, although it differs from that species in having reduced thorns and a wider peristome. UnlikeN. bicalcarata, this hybrid inhabits open areas with sandy substrates.[11]
This relatively rare natural hybrid is sometimes found growing among populations ofN. bicalcarata andN. rafflesiana. It is intermediate in form between its parent species.
Charles Clarke reported a single plant displaying characters intermediate between those ofN. bicalcarata,N. rafflesiana andN. mirabilis var.echinostoma, and growing among populations of these species. It is likely a complex hybrid, although this cannot be proven without the use ofmolecular techniques.[11]
Nepenthes bicalcarata may be cultivated in a similar manner to other members of the genus, though it requires relatively hot and humid conditions.[25][62] It needs large pots to do well, and temporary halts in growth are often due to becoming root-bound. Re-potting to a larger pot will often result in a rapid size increase. Under satisfactory conditions, this plant will grow quite fast for aNepenthes, reaching a large size relatively rapidly.
Despite naturally occurring in peat swamp forests,N. bicalcarata has been successfully grown in a completely inorganic substrate consisting of one part each of Seramis clay perls, lava gravel, and Lecaton expanded clay perls.[63]
Nepenthes bicalcarata has been artificially crossed withN. hirsuta. A particularly robust-pitcheredcultivar of this hybrid was namedNepenthes 'Hortulanus Otten', in honour of Karel Otten, former curator of the Botanic Garden inGhent, Belgium.[64]
A cultivar of the artificial crossN. bicalcarata ×N. × dyeriana was registered in 1988 under the nameNepenthes 'Nina Dodd'. It is named after a relative of Cliff Dodd, who created the hybrid.[65]
Two further cultivars of manmade hybrids involvingN. bicalcarata have been named. These areNepenthes 'Bella' ((N. ampullaria ×N. bicalcarata) ×N. truncata) andNepenthes 'Rapa' (N. ampullaria ×N. bicalcarata).[66] However, both of these names are not established, as they were published without a description.[6]
