Nepenthes × Trichocarpa

''Nepenthes'' ( ) is a genus of carnivorous plants, also known as tropical pitcher plants, or monkey cups, in the monotypic family Nepenthaceae. The genus includes about 170 species, and numerous natural and many cultivated hybrids. They are mostly liana-forming plants of the Old World tropics, ranging from South China, Indonesia, Malaysia, and the Philippines; westward to Madagascar (two species) and the Seychelles (one); southward to Australia (four) and New Caledonia (one); and northward to India (one) and Sri Lanka (one). The greatest diversity occurs on Borneo, Sumatra, and the Philippines, with many endemic species. Many are plants of hot, humid, lowland areas, but most are tropical, montane plants, receiving warm days but cool to cold, humid nights year-round. A few are considered tropical alpine, with cool days and nights near freezing. The name "monkey cups" refers to the fact that monkeys were once thought to drink rainwater from the pitchers.

Description

''Nepenthes'' species usually consist of a shallow root system and a prostrate or climbing stem, often several metres long and up to or more, and usually or less in diameter, although this may be thicker in a few species (e.g. '' N. bicalcarata''). From the stems arise alternate, sword-shaped leaves with entire leaf margins. An extension of the midrib (the tendril), which in some species aids in climbing, protrudes from the tip of the leaf; at the end of the tendril the pitcher forms. The pitcher starts as a small bud and gradually expands to form a globe- or tube-shaped trap.

The trap contains a fluid of the plant's own production, which may be watery or more viscous, and is used to drown the prey. This fluid contains viscoelastic biopolymers that may be crucial to the retention of insects within the traps of many species. The viscoelastic fluid in the pitchers is especially effective in the retention of winged insects. The trapping efficiency of this fluid remains high, even when significantly diluted by water, as inevitably happens in wet conditions.

The lower part of the trap contains glands that absorb nutrients from captured prey. Along the upper inside part of the trap is a slick, waxy coating, which makes the escape of its prey nearly impossible. Surrounding the entrance to the trap is a structure called the peristome (the "lip"), which is slippery and often quite colorful, attracting prey, but offering an unsure footing. The prey-capture effectiveness of the peristome is further enhanced in moist environments, where condensation may cause a thin water film to form on the surface of the peristome. When wet, the slippery surface of the peristome causes insects to "aquaplane", or slip and fall, into the pitcher. Above the peristome is a lid (the operculum); in many species, this keeps rain from diluting the fluid within the pitcher, the underside of which may contain nectar glands that attract prey.

''Nepenthes'' species usually produce two types of pitchers, known as leaf dimorphism. Appearing near the base of the plant are the large, lower traps, which typically sit on the ground. The upper or aerial pitchers are usually smaller, coloured differently, and possess different features from the lower pitchers. These upper pitchers usually form as the plant reaches maturity and the plant grows taller. To keep the plant steady, the upper pitchers often form a loop in the tendril, allowing it to wrap around nearby support. In some species (e.g. '' N. rafflesiana''), different prey may be attracted by the two types of pitchers. This varied morphology also often makes identification of species difficult.

Prey usually consists of insects, but the largest species (e.g. '' N. rajah'' and ''N. rafflesiana'') may occasionally catch small vertebrates, such as "frogs, birds, and small mammals". Records of cultivated plants trapping small birds have been made. Flowers occur in racemes or more rarely in panicles with male and female flowers on separate plants. Three species have symbiotic relationships with treeshrews, which eat the nectar produced by the plant and defecate into the pitchers, providing valuable nutrients.

''Nepenthes'' are insect-pollinated, the primary agents being flies (including blow flies, midges, and mosquitoes), moths, wasps, and butterflies.Clarke, C.M. 2001. ''Nepenthes of Sumatra and Peninsular Malaysia''. Natural History Publications (Borneo), Kota Kinabalu. Their smells can range from sweet to musty or fungus-like. Seed is typically produced in a four-sided capsule which may contain 50–500 wind-distributed seeds, consisting of a central embryo and two wings, one on either side (though '' N. pervillei'' differs).

The genus is cytologically diploid, with all studied species having a chromosome number of ''2n''=80. This high number is thought to reflect paleopolyploidy (likely 8x or 16x).

Taxonomy

About 170 species of ''Nepenthes'' are currently recognised as valid. This number is increasing, with several new species being described each year.

Etymology

The genus name ''Nepenthes'' was first published in 1737 in Carl Linnaeus's ''Hortus Cliffortianus''. It references a passage in Homer's ''Odyssey'', in which the potion "Nepenthes pharmakon" is given to Helen by an Egyptian queen. "'' Nepenthes''" () literally means "without grief" ( ''nē'' = "not", ''penthos'' = "grief") and, in Greek mythology, is a drug that quells all sorrows with forgetfulness. Linnaeus explained:

If this is not Helen's ''Nepenthes'', it certainly will be for all botanists. What botanist would not be filled with admiration if, after a long journey, he should find this wonderful plant. In his astonishment, past ills would be forgotten when beholding this admirable work of the Creator! ranslated from Latin by Harry Veitch">Harry_Veitch.html" ;"title="ranslated from Latin by Harry Veitch">ranslated from Latin by Harry Veitch/blockquote>

The plant Linnaeus described was ''N. distillatoria'', called'' bāndurā'' (බාඳුරා), a species from Sri Lanka.

''Nepenthes'' was formally published as a generic name in 1753 in Linnaeus's famous ''Species Plantarum">genus">generic name in 1753 in Linnaeus's famous ''Species Plantarum'', which established botanical nomenclature as it exists today. ''Nepenthes distillatoria'' is the type species of the genus.

The name "monkey cups" was discussed in the May 1964 issue of ''National Geographic'', in which Paul A. Zahl wrote:

The carriers called them "monkey cups", a name I had heard elsewhere in reference to ''Nepenthes'', but the implication that monkeys drink the pitcher fluid seemed farfetched. I later proved it true. In Sarawak, I found an orangutan that had been raised as a pet and later freed. As I approached it gingerly in the forest, I offered it a half-full pitcher. To my surprise, the ape accepted it, and with the finesse of a lady at tea, executed a delicate bottoms-up.

The plants are often called ''kantong semar'' (Semar's pocket) in Indonesia and ''sako ni Hudas'' ( Judas' money bag) in the Philippines.

Evolution and phylogeny

An absence of evidence of intermediate species, fossil or living (i.e. a missing link), does not allow forming a phylogenetic timeline for the development of the distinctive traits of modern ''Nepenthes'', which include its relatively rare strict dioecy and carnivorous pitchers. Although ''Nepenthes'' is distantly related to several modern genera, among these, even the carnivorous relatives he sundews (''Drosera''), Venus flytrap (''Dionaea muscipula">Drosera.html" ;"title="he sundews (''Drosera">he sundews (''Drosera''), Venus flytrap (''Dionaea muscipula''), waterwheel plant (''Aldrovanda''), and dewy pine (''Drosophyllum'')], all lack those traits. Among known ''Nepenthes'', no protomodern characteristics or large variations are found, which suggests that all extant species radiated from a single close ancestor bearing all the modern traits. Phylogenetic comparisons of the chloroplast '' matK ''gene sequences between ''Nepenthes'' species and with related species support this conclusion, long genetic distance between ''Nepenthes'' and others, and abruptly diverging "pom-pon" grouping of the ''Nepenthes'' species .

Fossilized pollen of ''Nepenthes''-like plants living on the northern Tethys Sea from 65 to 35 million years ago indicates that then-warmer Europe may have been where the proto-''Nepenthes'' developed, and then escaped to Asia and India as Africa collided with Europe and the ensuing climate change wiped out the ancestral species in the original habitat. About 20 million years ago, Borneo, Sumatra, and Sulawesi and possibly even the Philippines were connected to mainland Asia, providing a bridge for the colonization of most sites of ''Nepenthes'' species radiation. The extensive land bridges in the area 20,000 years ago during the ice age would have provided access to the remaining sites of ''Nepenthes'' populations in Oceania. The main complication with this hypothesis is the presence of ''Nepenthes'' on the distant islands of Seychelles and Madagascar. The seeds were thought to have been transferred by seabirds and shorebirds, which rest during their migrations in swampy habitats and may have inadvertently picked up the seeds. This hypothesis is possibly reinforced by the success of the lowland swamp-dwelling '' N. distillatoria'' in colonizing so many locations.

Distribution and habitat

The genus ''Nepenthes'' is mostly found within the Malay Archipelago, with the greatest biodiversity found on Borneo, Sumatra, and the Philippines, especially in the Borneo montane rain forests. The full range of the genus includes Madagascar ('' N. madagascariensis'' and '' N. masoalensis''), the Seychelles ('' N. pervillei''), Sri Lanka ('' N. distillatoria''), and India ('' N. khasiana'') in the west to Australia ('' N. mirabilis'', '' N. rowanae'', '' N. parvula'', and '' N. tenax'') and New Caledonia ('' N. vieillardii'') in the southeast. Most species are restricted to very small ranges, including some found only on individual mountains. These limited distributions and the inaccessibility of the regions often means some species go decades without being rediscovered in the wild (e.g. '' N. deaniana'', which was rediscovered 100 years after its initial discovery). About 10 species have population distributions larger than a single island or group of smaller islands. ''Nepenthes mirabilis'' has the distinction of being the most widely distributed species in the genus, ranging from Indochina and throughout the Malay Archipelago to Australia.McPherson, S.R. 2009. ''Pitcher Plants of the Old World''. 2 volumes. Redfern Natural History Productions, Poole.

Because of the nature of the habitats that ''Nepenthes'' species occupy, they are often graded as either lowland or highland species, depending on their altitude above sea level, with the rough delineation between lowland and highland. Species growing at lower altitudes require continuously warm climates with little difference between day and night temperatures, whereas highland species thrive when they receive warm days and much cooler nights. '' Nepenthes lamii'' grows at a higher altitude than any other in the genus, up to .

Most ''Nepenthes'' species grow in environments that provide high humidity and precipitation and moderate to high light levels. A few species, including '' N. ampullaria'', prefer the dense, shaded forests, but most other species thrive on the margins of tree/shrub communities or clearings. Some species (e.g. ''N. mirabilis'') have been found growing in clear-cut forest areas, roadsides, and disturbed fields. Other species have adapted to growing in savanna-like grass communities. The soils in which ''Nepenthes'' species grow are usually acidic and low in nutrients, being composed of peat, white sand, sandstone, or volcanic soils. Exceptions to these generalities include species that thrive in soils with high heavy metal content (e.g. '' N. rajah''), on sandy beaches in the sea spray zone (e.g. '' N. albomarginata''). Other species grow on inselbergs and as lithophytes, while others, such as '' N. inermis'', can grow as epiphytes with no soil contact.

Ecological relationships

The most obvious interaction between ''Nepenthes'' species and their environments, including other organisms, is that of predator and prey. ''Nepenthes'' species attract their prey through active production of attractive colours, sugary nectar, and sweet scents. From this relationship, the plants primarily gain nitrogen and phosphorus to supplement their nutrient requirements for growth, given these soil nutrients are typically lacking. The most frequent prey is an abundant and diverse group of arthropods, with ants and other insects topping the menu. Other arthropods found frequently include spiders, scorpions, and centipedes, while snails and frogs are more unusual, but not unheard of. The most uncommon prey for ''Nepenthes'' species includes rats found in ''N. rajah''. The composition of prey captured depends on many factors, including location, but can incorporate hundreds of individual insects and many different species. While many ''Nepenthes'' species are generalists in what they capture, at least one, '' N. albomarginata'', has specialised and almost exclusively traps termites and produces nearly no nectar. ''Nepenthes albomarginata'' gains its name from the ring of white trichomes directly beneath the peristome. These trichomes—or "hairs"—are palatable to termites and will attract them to the pitcher. In the course of collecting the edible trichomes, hundreds or thousands of termites will fall into the pitcher.

Symbioses

'' N. bicalcarata'' provides space in the hollow tendrils of its upper pitchers for the carpenter ant '' Camponotus schmitzi'' to build nests. The ants take larger prey from the pitchers, which may benefit ''N. bicalcarata'' by reducing the amount of putrefaction of collected organic matter that could harm the natural community of infaunal species that aid the plant's digestion.Clarke, C.M. 1997. ''Nepenthes of Borneo''. Natural History Publications (Borneo), Kota Kinabalu.

'' N. lowii'' has also formed a dependent relationship, but with vertebrates instead of insects. The pitchers of ''N. lowii'' provide a sugary exudate reward on the reflexed pitcher lid (operculum) and a perch for tree shrew species, which have been found eating the exudate and defecating into the pitcher. A 2009 study, which coined the term "tree shrew lavatories", determined between 57 and 100% of the plant's foliar nitrogen uptake comes from the faeces of tree shrews. Another study showed the shape and size of the pitcher orifice of ''N. lowii'' exactly match the dimensions of a typical tree shrew (''Tupaia montana'').Walker, M. 2010
Giant meat-eating plants prefer to eat tree shrew poo
''BBC Earth News'', March 10, 2010. A similar adaptation was found in '' N. macrophylla'', '' N. rajah'', '' N. ampullaria'', and is also likely to be present in '' N. ephippiata''.

Similarly, '' N. hemsleyana'', which is native to Borneo, has a symbiotic partnership with Hardwicke's woolly bat. During the day, a bat may roost above the digestive fluid inside the pitcher. While a bat is inside, it may defaecate, with the plant gaining nitrogen from the droppings. Further research has discovered that the shape and design of the pitcher has evolved to be an acoustic reflector to make it easier for bats to echo-locate, and distinguishes it from other closely related species that don't make good roosts.

Infauna

Organisms that spend at least part of their lives within the pitchers of ''Nepenthes'' species are often called ''Nepenthes'' infauna. The most common infaunal species, often representing the top trophic level of the infaunal ecosystem, are many species of mosquito larvae. Other infaunal species include fly and midge larvae, spiders, mites, ants, and even a species of crab ('' Geosesarma malayanum''). Many of these species specialise to one pitcher plant species and are found nowhere else. These specialists are called nepenthebionts. Others, often associated with but not dependent on ''Nepenthes'' species, are called nepenthophiles. Nepenthexenes, on the other hand, are rarely found in the pitchers, but will often appear when putrefaction approaches a certain threshold, attracting fly larvae that would normally not be found in the pitcher infaunal community. The complex ecological relationship between pitcher plants and infauna is not yet fully understood, but the relationship may be mutualistic: the infauna is given shelter, food, or protection, and the plant that harbours the infauna receives expedited breakdown of captured prey, increasing the rate of digestion and keeping harmful bacterial populations repressed.

Antimicrobial properties

''Nepenthes'' digestive fluids are sterile before pitchers open and contain secondary metabolites and proteins that act as bactericides and fungicides after the pitcher opens. While the digestive fluid is being produced, the pitcher is not yet open, so there is no chance of microbial contamination. During pitcher development, at least 29 digestive proteins including proteases, chitinases, pathogenesis-related proteins and thaumatin-like proteins are produced in the pitcher fluid. In addition to breaking down prey, these can act as antimicrobial agents. When the pitchers open, the fluid is exposed to bacteria, fungal spores, insects and rain. Often pitchers have a lid that covers the trap, excepting a few (e.g. '' N. lowii'', '' N. attenboroughii'' and '' N. jamban''), preventing rain water from entering. The lid inhibits rainwater from diluting the digestive fluid. Once the bacteria and fungi enter the fluid, secondary metabolites are produced in addition to antimicrobial proteins. Naphthoquinones, a class of secondary metabolite, are commonly produced, and these either kill or inhibit the growth and reproduction of bacteria and fungi. This adaptation could have evolved since ''Nepenthes'' plants that could produce secondary metabolites and antimicrobial proteins to kill bacteria and fungi were most likely more fit. Plants that produced antimicrobial compounds could prevent loss of valuable nutrients gained from insects within the pitcher. Since ''Nepenthes'' cannot digest certain bacteria and fungi, the bactericides and fungicides allow plants to maximize nutrient uptake.

Botanical history

The earliest known record of ''Nepenthes'' dates back to the 17th century. In 1658, French colonial governor Étienne de Flacourt published a description of a pitcher plant in his seminal work ''Histoire de la Grande Isle de Madagascar''. It reads:

It is a plant growing about 3 feet high which carries at the end of its leaves, which are 7 inches long, a hollow flower or fruit resembling a small vase, with its own lid, a wonderful sight. There are red ones and yellow ones, the yellow being the biggest. The inhabitants of this country are reluctant to pick the flowers, saying that if somebody does pick them in passing, it will not fail to rain that day. As to that, I and all the other Frenchmen did pick them, but it did not rain. After rain these flowers are full of water, each one containing a good half-glass. ranslated from French in ''Pitcher-Plants of Borneo''">Pitcher-Plants_of_Borneo.html" ;"title="ranslated from French in ''Pitcher-Plants of Borneo">ranslated from French in ''Pitcher-Plants of Borneo''ref name=P&L />

Flacourt called the plant ''Amramatico'', after a local name. More than a century later, this species was Species description">formally described