Carnivorous plant

Darlingtonia: note the small entrance to the trap underneath the swollen 'balloon', and the colourless patches that confude prey trapped inside

nutrients (but not energy) by trapping and consuming animals, especially insects and other arthropods. Carnivorous plants usually grow in places where the soil is thin or poor in nutrients, especially nitrogen, such as acidic bogs and rock outcroppings. Charles Darwin wrote the first well-known treatise on carnivorous plants in 1875.

Trapping mechanisms

There are five basic trapping mechanisms exploited by carnivorous plants. These are:

• Pitfall traps (pitcher plants), which trap prey in a rolled leaf that contains a pool of digestive enzymes;
• Flypaper traps, which trap prey using a sticky mucilage;
• Snap traps, which trap prey with rapid leaf movements;
• Bladder traps, which suck in prey with a bladder that generates an internal vacuum; and
• Lobster-pot traps, which use inward pointing hairs to force prey to move towards a digestive organ.

These traps may also be classified as active or passive. For example, there are both passive flypapers, such as Triphyophyllum, which secrete mucilage, but whose leaves do not grow or move in response to prey capture; and there are also active flypapers, such as most sundews, whose leaves undergo rapid growth, aiding in the retention and digestion of prey.

Pitfall traps

Pitfall traps have evolved independently on at least four occasions. The simplest pitfall traps are probably those of Heliamphora, the marsh (or sun) pitcher plant. In this genus, the leaves are quite clearly evolutionarily derived from a simple rolled leaf, whose margins have been sealed together. These plants live in areas of high rainfall in South America (such as Mount Roraima), and consequently have a problem ensuring their pitchers do not overflow. To counteract this problem, natural selection has favoured the evolution of an overflow, similar to that of a bathroom sink: there is a small gap in the zipped up leaf margins that allows excess water to flow out of the pitcher.

Heliamphora is a member of the Sarraceniaceae, a New World family in the order Ericales (heathers and allies). Heliamphora is limited to South America, but the family contains two other genera, Sarracenia and Darlingtonia, which are endemic to Florida (for the most part) and California respectively. Sarracenia is the pitcher plant genus most commonly encountered in cultivation, and are usually known as trumpet pitchers. S. purpurea (the huntman's cup) has a more cosmopolitan distribution.

In the genus Sarracenia, the problem of pitcher overflow is solved by the evolution of an operculum, which is essentially a flared leaflet that covers the opening of the rolled-leaf tube, and protects it from rain. Possibly because of this improved waterproofing, species of Sarracenia secrete enzymes such as proteases and phosphatases into the digestive fluid at the bottom of the pitcher: Heliamphora relies on bacterial digestion alone. These enzymes digest the proteins and nucleic acids in the prey, releasing amino acids and phosphate ions, which the plant absorbs. Darlingtonia californica, the cobra plant, possesses an adaptation also found in Sarracenia psittacina and to a lesser extent in Sarracenia minor: the operculum is balloon-like, and almost seals the opening to the tube. This balloon-like chamber is pitted with areolae, which are chlorophyll-free patches through which light can penetrate. Insects (mostly ants) get into the chamber via the opening, which is underneath the balloon, and once inside, tire themselves out trying to escape from these false exits, until they eventaully fall into the tube. Prey access is increased by the 'fangs' (outgrowths of the operculum), which give the plant its name. Seedling Sarracenia species also have long, overhanging opercular outgrowths: Darlingtonia may therefore be an example of neoteny.

The second major group of pitcher plants are the monkey cups or tropical pitcher plants of the genus Nepenthes. In the seventy or so species of this genus, the pitcher is borne at the end of a tendril, which grows as an extension to the midrib of the leaf. Most species catch insects, although the larger ones, particularly N. rajah, will also occasionally take small mammals and reptiles. These pitchers represent a convenient source of food to small insectivores: N. bicalcarata possesses two sharp thorns that project from the base of the operculum over the entrance to the pitcher, which provide some protection from raids by freeloading mammals.

The pitfall trap has evolved in at least two other groups. Cephalotus follicularis, the Albany pitcher plant, is a small pitcher plant from Western Australia, with moccasin-like pitchers. In this species, the rim of the pitcher's opening (the peristome) is particularly pronounced, and both secretes nectar, and provides a thorny overhang to the opening, which prevents trapped insects from climbing out. The lining of most pitcher plants is very waxy, which provides a very uncertain footing for insects. The insects are often attracted by nectar bribes secreted by the peristome, and by bright flower-like anthocyanin patterning. In at least one species (Sarracenia flava), the nectar bribe is laced with coniine, a toxic alkaloid, which probably increases the efficiency of the traps by intoxicating the prey items.

The final carnivore with a pitfall-like trap is the bromeliad, Brocchinia reducta. Like most relatives of the pineapple, this species has an urn, formed from the tightly-packed waxy leaf bases of the strap-like leaves. In most bromeliads, water collects readily in this urn, and may provide habitats for frogs, insects and (more usefully from the plant's point of view), diazotrophic (nitrogen-fixing) bacteria. In Brocchinia, the urn is specialised as an insect-trap, with a population of digestive bacteria, and a loose, waxy lining.

Flypaper traps

The flypaper traps are those whose trapping mechanism is based on a sticky mucilage, or glue. The leaf of flypaper traps is studded with mucilage-secreting glands, which may either be short and nondescript (like those of the butterworts), or long and mobile (like those of many sundews). Flypapers have evolved independently at least five times.

In the genus Pinguicula, the mucilage glands are quite short (sessile), and the leaf, whilst shiny (giving the genus its common name of 'butterwort'), does not appear particularly carnivorous. However, this belies the fact that the leaf is an extremely effective trap of small flying incests (such as fungus gnats), whose surface responds to prey by relatively rapid growth. This thigmotropic growth may involve rolling of the leaf blade (to prevent rain from splashing the prey off the leaf surface), or 'dishing' of the surface under the prey, to form a shallow digestive pit.

The sundew genus (Drosera) consists of over 100 species of active flypapers, whose mucilage glands are borne at the end of long tentacles, which frequently grow fast enough in response to prey (thigmotropism) to aid the trapping process. The tentacles of D. burmanii are capable of bending 180° in only a minute or so. Sundews are extremely cosmopolitan, and are found on all the continents except the Antarctic mainland. They are probably at their most diverse in Australia, the home of the large subgroup of pygmy sundews, such as D. pygmaea, and a number of tuberous sundews such as D. peltata. These species are so dependent on insect sources of nitrogen that they generally lack the enzyme (nitrate reductase), which most plant require to assimilate soilborne nitrate into organic chemicals.

Closely related to Drosera is the Portuguese dewy pine, Drosophyllum, which differs from the sundews in being passive: the leaves are incapable of rapid movement or growth. Unrelated, but similar in habit, are the Australian rainbow plants (Byblis). Drosophyllum is unusual amongst carnivores in that it grows under near-desert conditions: almost all other carnivores are either bog plants or grow in moist tropical areas.

The final flypaper is Triphyophyllum peltatum. This plant is usually encountered as a liana, however, in its juvenile phase, the plant is carnivorous: this may be related to a requirement for specific nutrients for flowering.

Snap traps

There are only two snap-traps, which are believed to have had a similar common ancestor. These are the Venus flytrap (Dionaea muscipula) and the waterwheel plant (Aldrovanda vesiculosa). Aldrovanda is aquatic, and specialised in catching small aquatic invertebrates; Dionaea is terrestrial and catches mostly flies. The traps are very similar: they have leaves whose terminal section is formed into two lobes, hinged along the midrib. Trigger hairs inside the trap lobes are sensitive to touch. When the trigger hairs are bent, stretch-gated ion channels in the membranes of cells at the base of the trigger hair open, generating an action potential, which propagates to cells in the midrib. These cells respond by pumping out potassium ions. Water follows by osmosis, and the cells in the midrib collapse, allowing the lobes (which are held under tension) to snap shut. This whole process takes less than a second. In the Venus flytrap, spurious closure (in response to raindrops and blown-in debris) is prevented by the leaf's having a simple memory: for the lobes to shut, two stimuli are required, between one half and 30 seconds apart.

The snapping of the leaves is a case of thigmonasty (undirected movement in response to touch). Further stimulation of the lobe's internal surfaces by the struggling insects causes the lobes to grow together (towards the prey: thigmotropism), sealing the lobes hermetically, and forming a stomach in which digestion occurs over a period of one to two weeks. Leaves can be reused three or four times before they become unresponsive to stimulation.

Bladder traps

Bladder traps are exclusive to the genus Utricularia, or bladderworts. These possess bladders (or vesicula), which pump ions out of their interiors. Water follows the ions by osmosis, and this generates a partial vacuum inside the bladder. The bladder has a small opening, sealed by a hinged door. In aquatic species, the door has a pair of long trigger hairs. Aquatic invertebrates (such as Daphnia) that touch these hairs deform the door by lever action: this releases the vacuum, and sucks the invertebrate into the bladder, where it is digested. Many species of Utricularia (such as U. sandersonii) are terrestrial, growing on waterlogged soil, and their trapping mechanism is triggered in a slightly different manner.

Lobster-pot traps

Lobster pots are found in Sarracenia psittacina, and more elegantly, in Genlisea, the corkscrew plants. In these plants, which appear to specialise in aquatic protozoa, a Y-shaped modified leaf allows entrance to prey, but not exit. This is achieved by inward-pointing hairs, which force the prey to move in a particular direction. Prey items entering the spiral entrance that coils around the upper two arms of the 'Y' are forced to move inexorably towards a 'stomach' in the lower arm of the 'Y', where they are digested.

Borderline carnivores

To be a fully fledged carnivore, a plant must attract, kill, and digest prey; and it must benefit from absorbing the products of the digestion (mostly amino acids and ammonium ions). There are a number of plants which fail on one or more of these counts: whether these count as carnivorous is a matter of definition, although to many horticulturalists, it is a matter of taste. From this, it should be obvious that there is a spectrum of carnivory: from 'non-carnivores' like cabbages, through borderline carnivores, to the true carnivores, including both unspecialised and simple traps, like Heliamphora, to extremely specialised and complex traps, like the Venus flytrap.

The borderline carnivores of most interest are Roridula and Catopsis berteroniana. Catopsis is a borderline carnivorous bromeliad, like Brocchinia; however, Roridula has a more intricate relationship with its 'prey'. The plants in this genus produce sticky leaves with mucilage-tipped glands, and look extremely similar to some of the larger sundews. However, they do not directly benefit from the insects they catch. Instead, they form a mutualistic symbiosis with a species of assassin bug (Pameridea), which eat the trapped insects: the plant benefits by absorbing nutrients from the bugs' faeces.

A number of species in the Martyniaceae (previously the Pedaliaceae), such as Ibicella lutea have sticky leaves that trap insects; however, these plants have not been shown conclusively to be carnivorous. Likewise, the seeds of Shepherd's Purse, urns of Paepalanthus bromelioides and bracts of Passiflora foetida appear to trap and kill insects, but their classification as carnivores is contentious.

Evolution

Elucidating the evolution of carnivorous plants is made difficult by the paucity of their fossil record. Very few fossils have been found, and almost all are either seed or pollen. However, much can be deduced from the structure of current traps. Pitfall traps are clearly derived from rolled leaves (the vascular tissues of Sarracenia show this quite clearly), and flypapers show a simple evolutionary gradient from sticky, non-carnivorous leaves, through passive flypapers to active forms. The snap-traps are thought to be derived from very fast-moving flypapers which became less reliant on glue.

There are over a quarter of a million species of flowering plants, but of these, only around five hundred are known to be carnivorous. True carnivory has probably evolved independently at least ten times; however, some of these 'independent' groups are probably descended from a recent common ancestor with a predisposition to carnivory. Some groups (the Ericales and Caryophyllales) seem particularly fertile ground for carnivorous preadpatation, although in the former case, this may be more to do with the ecology of the group than its morphology.

It has been suggested that all of the various trap types are modifications of a similar basic structure - the hairy leaf. Hairy (or more specifically, stalked-glandular) leaves have the ability to catch and retain drops of rainwater (especially if shield-shaped or peltate) in which bacteria can breed. Insects that land on the leaf can become mired by the surface tension of the water, and suffocate. The bacteria then begin the process of decay, releasing nutrients from the corpse, which the plant can absorb through its leaves. This foliar feeding can be observed in most non-carnivorous plants. Plants that were better at retaining insects or water therefore had a selective advantage, because they had access to more nutrients than less efficient plants. Rainwater can be retained by cupping the leaf, leading to pitfall traps. Alternatively, insects can be retained by making the leaf stickier by the production of mucilage, leading to flypaper traps.

The pitfall traps may have evolved simply by selection pressure for the production of more deeply cupped leaves, followed by 'zipping up' of the margins and subsequent loss of most of the hairs, except at the bottom, where they help retain prey.

The lobsterpot traps of Genlisea can be interpreted as pitchers formed from a Y shaped leaf, that later specialised on ground dwelling prey. The twist is an adaptation that displays as much trapping surface as possible in all directions when buried in moss. In this case the hairs were also retained, but to a greater extent, since the trap was no longer held vertically, and could not rely on gravity to keep its prey in.

The traps of the bladderworts, are more difficult to explain, but they may be derived from pitchers that specialised in aquatic prey when flooded, like Sarracenia psittacina does today. Escaping prey items in terrestrial pitchers have to climb or fly out of a trap, and both of these can be easily prevented by wax and tube narrowness. However, a flooded trap has to be swum out of, so in Utricularia, a one way lid may have developed to form the door of a proto-bladder. Later, this may have become active by the evolution of a partial vacuum inside the bladder, tripped by prey brushing against trigger hairs on the door of the bladder.

Flypaper traps include the various true flypapers and the snap traps of Aldrovanda and Dionaea. The production of sticky mucilage is found in many non-carnivorous genera, so it is not difficult to see how the passive glue traps in Byblis and Drosophyllum evolved.

The active glue traps require a little more explanation. Rapid plant movement can be due to actual rapid growth, or it can be due to rapid changes in cell turgor, which allow cells to expand or contract by quickly altering their water content. Slow-moving flypapers like Pinguicula use growth, but the Venus flytrap uses more rapid turgor changes. In the Venus flytrap, the movement is so rapid that glue has become unnecessary, and hence is no longer produced. The stalked glands that once made it (and are so evident in Drosera) have become the teeth and trigger hairs - an example of natural selection hijacking preexisting structures for entirely new functions.

Recent taxonomic analysis of the relationships within the Caryophyllales indicate that the Droseraceae, Triphyophyllum, Nepenthaceae and Drosophyllum, whilst closely related, are embedded within a larger clade that includes non-carnivorous groups such as the tamarisks, Ancistrocladaceae, Polygonaceae and Plumbaginaceae. Interestingly, the tamarisks possess specialised salt-excreting glands on their leaves, as do several of the Plumbaginaceae (such as the sea lavender, Limonium). Many of the Plumbaginaceae also have stalked, vascularised glands that secrete mucilage on their calyces and aid in seed dispersal and possibly in protecting the flowers from parasitic insects. It is not unlikely that these are homologous with the tentacles of the carnivorous genera. The balsams (such as Impatiens), which are closely related to the Sarraceniaceae and Roridula, similarly possess stalked glands.

The only genera that are unlikely to have descended from a hairy leaf of some sort are the carnivorous bromeliads (Brocchinia and Catopsis). These plants have just used the urn that is a fundamental part of the structure of a bromeliad for a new purpose, and built on it by the production of wax, enzymes and the other paraphernalia of carnivory.

Ecology and modelling of carnivory

Carnivorous plants are widespread but rather rare: there are only about 500 species, out of about 250, 000 flowering plants. They are almost entirely restricted to habitats such as bogs, where soil nutrients are extremely limiting, but where sunlight and water are readily available. Only under such extreme conditions is carnivory favoured to an extent that makes the adaptations obvious.

The archetypal carnivore, the Venus flytrap, grows under quite extreme environmental conditions. The soils in which it grows have nitrate and calcium levels that are almost too low to measure. This poses an obvious problem since nitrogen is essential for protein synthesis and calcium for cell wall stiffening. Soil phosphate and iron levels are also very low, phosphate being essential for nucleic acid synthesis, and iron for chlorophyll synthesis. The soil is often waterlogged, which favours the production of toxic ions such as ammonium, and its pH is an extremely acidic 4 to 5. Ammonium can be used as a source of nitrogen by plants, but its extreme toxicity means that concentrations high enough to fertilise are also high enough to cause damage.

However, the habitat is warm, sunny, constantly moist, and the plant experiences relatively little competition from low growing Sphagnum moss. This sort of habitat is typical of many carnivorous plants, and carnivores have a popular reputation as bog plants. However, they are also found in very atypical habitats too. Drosophyllum lusitanicum is found around desert edges and Pinguicula valisneriifolia on limestone (calcium rich) cliffs. Any model that attempts to explain carnivory must explain both why carnivores are so often restricted to wet, soggy, sunny sites, and how can they can survive away from them.

In all the studied cases, carnivory allows plants to grow and reproduce using animals as a source of nitrogen, phosphorus and (possibly) potassium, when the usual sources in the soil are absent or limiting. However, there is a spectrum of dependency on animal prey. Pygmy sundews are unable to use nitrate from soil because they lack the necessary enzymes (nitrate reductase in particular), so they are almost entirely dependent on animal prey. Common butterworts (Pinguicula vulgaris) can use inorganic sources of nitrogen better than organic sources, but a mixture of both gives better growth than either alone. European bladderworts seem able to use either source equally well. Animal prey makes up for deficiencies in soil nutrients, but to different extents in different plants.

Plants use their leaves to intercept sunlight. The light energy is used to reduce carbon dioxide from the air with electrons from water, to make sugars (and other biomass), and a waste product, oxygen, in the process of photosynthesis. Leaves also respire, in a very similar way to animals, by burning their biomass to generate chemical energy. This energy is temporarily stored in the form of ATP (adenosine triphosphate), which acts as an energy currency for metabolism in all living things. As a waste product, respiration produces carbon dioxide.

For a plant to grow, it must photosynthesise more than it respires. If a plant respires more than it photosynthesises, then it will eventually burn up all its available biomass, and die. The potential for plant growth is net photosynthesis. Net photosynthesis is the total gross gain of biomass by photosynthesis, minus the biomass burnt up by respiration. Understanding carnivory requires a cost-benefit analysis of these factors.

In carnivorous plants, the leaf is not just used to photosynthesise, but also as a trap. Unfortunately, changing the leaf shape to make it a better trap generally makes it less efficient at photosynthesis. For example, pitchers have to be held upright, so that only their opercula directly intercept light. The plant also has to expend extra energy on non-photosynthetic structures like glands, hairs, glue and digestive enzymes. The energy source for these things is ATP, so the plant has to respire more of its biomass away to keep up with the demand for energy. Hence, a carnivorous plant will have both decreased photosynthesis and increased respiration, making the potential for growth small, and the cost of carnivory high.

The benefits of carnivory are the nitrogen and phosphorus harvested from the prey items. Being carnivorous allows the plant to grow better when the soil contains little nitrate or phosphate. In particular, an increased supply of nitrogen and phosphorus makes photosynthesis more efficient, because photosynthesis depends on the plant being able to synthesise very large amounts of the (nitrogen rich) enzyme Rubisco (ribulose-1,5-bis-phosphate carboxylase/oxygenase), which is the most abundant protein on Earth. The returns of carnivory are therefore more effective photosynthesis.

Clearly some sort of tradeoff occurs. It is intuitively clear that the Venus flytrap is more carnivorous than Triphyophyllum peltatum: the former is a full time moving snap-trap, the second is a part time, non-moving flypaper. But is the Venus flytrap more carnivorous than a pitcher plant? The energy 'wasted' by the plant in building and fuelling its trap is a suitable measure of the carnivory of the trap.

Using this measure of investment in carnivory, a model can be proposed. Above is a graph of carbon dioxide uptake (potential for growth) against trap respiration (investment in carnivory) for a leaf in a sunny habitat containing no soil nutrients at all. Respiration is a straight line sloping down under the horizontal axis (respiration produces carbon dioxide). Gross photosynthesis is a curved line above the horizontal axis: as investment increases, so too does the photosynthesis of the trap, because the leaf is receiving a better supply of nitrogen and phosphorus. However, this payoff does not last forever. Eventually some other factor (such as light intensity or carbon dioxide concentration) will become more limiting to photosynthesis than nitrogen or phosphorus supply. As a result, increasing the investment will not make the plant grow any better. The net uptake of carbon dioxide, and therefore the plant's potential for growth, must be positive for the plant to survive. There is a broad span of investment where this is the case, and there is also a non-zero optimum. Plants investing more or less than this optimum will be taking up less carbon dioxide than an optimal plant, and hence growing less well. These plants will be at a selective disadvantage. At zero investment the growth is zero, because a non-carnivorous plant cannot survive in a habitat with absolutely no soil borne nutrients. No real habitat is this stressful, so non-carnivores can survive in the same habitats as carnivores. In particular, Sphagnum is able to absorb the tiny amounts of nitrates and phosphates contained in rain very efficiently, and also forms symbioses with diazotrophic cyanobacteria.

In a habitat with abundant soil nutrients but little light (as shown above), the gross photosynthesis curve will be lower and flatter, because light will be more limiting than nutrients. A plant can grow at zero investment in carnivory; however, this is also the optimum investment for a plant, as any investment in traps reduces net photosynthesis (growth) to less than the net photosynthesis of a plant that obtains its nutrients from soil alone.

Carnivorous plants exist between these two extremes: the less limiting light and water are, and the more limiting soil nutrients are, the higher the optimum investment in carnivory, and hence the more obvious the adaptations will be to the casual observer.

The most obvious evidence for this model is that carnivorous plants tend to grow in habitats where water and light are abundant, and where competition is relatively low: the typical bog. Those that do not tend to be even more fastidious in some other way: Drosophyllum lusitanicum grows where there is little water, but it is even more extreme in its requirement for bright light and low disturbance than most other carnivores. Pinguicula valisneriifolia grows on soils with high levels of calcium, but requires strong illumination and lower competition than many butterworts.

In general, carnivorous plants are poor competitors, because they invest too heavily in structures that have no selective advantage in nutrient-rich habitats. They survive because they can put up with nutrient stresses much higher than non-carnivorous plants can: they succeed because other plants fail. Carnivores are to nutrients what cacti are to water. Carnivory only pays off when the nutrient stress is very high and light is abundant. When these conditions are not met, some plants give up carnivory temporarily. Sarracenia spp. produce flat, non-carnivorous leaves (phyllodes) in winter. Light levels are lower than in summer, so light is more limiting than nutrients, and carnivory does not pay. The lack of insects in winter exacerbates the problem. Damage to growing pitcher leaves will prevent them from forming proper pitchers, and again, the plant produces a phyllode instead: the production of an inefficient, damaged trap is not worth the energy.

Many other carnivores shut down in some season: tuberous sundews die back to tubers in the dry season, bladderworts die back to turions in winter, and non-carnivorous leaves are made by most butterworts and Cephalotus in the less favourable seasons. Part-time carnivory in Triphyophyllum peltatum may be due to an unusually high need for potassium at a certain point in the life cycle, just before flowering.

The more carnivorous a plant is, the more conventional its habitat is likely to be. Venus flytraps live in a very stereotypical, and very specialised habitat, whereas less carnivorous plants (Byblis, Pinguicula) are found in more unusual habitats (i.e. those typical for non-carnivores). Byblis and Drosophyllum both come from relatively arid regions, and are both passive flypapers, which is arguably the lowest maintenance trap form. Venus flytraps filter their prey using the teeth around the trap's edge, so that energy is not wasted on prey items that cost more to digest than they pay back. In any evolutionary situation, being as lazy as possible pays, because energy can be devoted to reproduction, and as far as evolution is concerned, short term benefits in reproduction will always outweigh long-term benefits in anything else.

Carnivory very rarely pays: even "carnivorous plants" avoid it when there is too little light, or an easier source of nutrients, and they use as few carnivorous features as are required at a given time or for a given prey item. There are very few habitats stressful enough to make using biomass to make trigger hairs and enzymes worthwhile. Many plants occasionally benefit from animal protein rotting on their leaves, but carnivory obvious enough for the casual observer to notice is rare.

The lack of carnivorous bromeliads is instructive here: bromeliads seem very well preadapted to carnivory; however, only one or two species are truly carnivorous. Most bromeliads are epiphytes, and most epiphytes grow in partial shade on tree branches. It is noteworthy that Brocchinia reducta is a ground dweller. By their very shape, bromeliads will benefit from increased prey derived nutrient input. In this sense, most bromeliads are probably carnivorous, but their habitats are too dark for more extreme, recognisable carnivory to evolve.

Classification

The classification of all flowering plants is currently in a state of flux. In the Cronquist system, the Droseraceae and Nepenthaceae were placed in the order Nepenthales, based on the radial symmetry of their flowers, and their possession of insect-traps. The Sarraceniaceae was placed either in the Nepenthales, or in its own order, the Sarraceniales. The Byblidaceae, Cephalotaceae, and Roridulaceae were placed in the Saxifragales; and the Lentibulariaceae in the Scrophulariales.

In more modern classification, such as that of the Angiosperm Phylogeny Group, the families have been retained, but they have been redistributed amongst several disparate orders. It is also recommended that Drosophyllum be considered as a monotypic family outside the rest of the Droseraceae, possibly more closely allied to the Dioncophyllaceae. The current recommendations are shown below (only carnivorous genera are listed):

Dicots

• Caryophyllales, (carnation order)
  • Dioncophyllaceae
    • Triphyophyllum, (a tropical liana)
  • Drosophyllaceae
    • Drosophyllum, (Portuguese dewy pine)
  • Droseracaeae, (sundew family)
    • Aldrovanda, (waterwheel plant)
    • Dionaea, (Venus flytrap)
    • Drosera, (sundews)
  • Nepenthaceae, (tropical pitcher-plant family)
    • Nepenthes, (tropical pitcher plants or monkey-cups, including Anurosperma)

• Ericales (heather order)
  • Roridulaceae
    • Roridula, (a borderline carnivore)
  • Sarraceniaceae (trumpet pitcher family)
    • Sarracenia, (North American trumpet pitchers)
    • Darlingtonia, (cobra plant)
    • Heliamphora, (sun or marsh pitchers)

• Lamiales, (mint order)
  • Byblidaceae
    • Byblis, (rainbow plants)
  • Lentibulariaceae, (bladderwort family)
    • Pinguicula, (butterworts)
    • Genlisea, (corkscrew plant)
    • Utricularia, (bladderworts, including Polypompholyx, the fairy aprons or pink petticoats)
  • Martyniaceae, (all borderline carvivores, related to the sesame plant)
    • Ibicella
• Oxalidales, (wood sorrel order)
  • Cephalotus, (Albany pitcher plant)

Monocots

• Poales, (grass order)
  • Bromeliales, (bromeliad or pineapple family)
    • Brocchinia, (a terrestrial bromeliad)
    • Catopsis, (a borderline carnivore)

Cultivation

Although different species of carnivorous plants have different requirements in terms of sunlight, humidity, soil moisture, etc., there are commonalities.

Most carnivorous plants require rain water, or water that has been distilled, deionised by reverse osmosis, or acidified using sulfuric acid. Common tap or drinking water contains minerals (particularly calcium salts) that will quickly build up and kill the plant. This is because most carnivorous plants have evolved in nutrient-poor, acidic soils and are consequently extreme calcifuges. They are therefore very sensitive to excessive soil-borne nutrients. Since most of these plants are found in bogs, almost all are very intolerant of drying. There are exceptions: tuberous sundews require a dry (summer) dormancy period, and Drosophyllum requires mush drier conditions than most.

Outdoor-grown carnivorous plants generally catch more than enough insects to keep themselves properly fed. Insects may be fed to the plants by hand to supplement their diet; however, carnivorous plants are generally unable to digest large non-insect food items; bits of hamburger, for example, will simply rot, and this may cause the trap, or even the whole plant, to die. A carnivorous plant that catches no insects at all will not die, but its growth will be impaired. In general, these plant are best left to their own devices: after underwatering with tap-water, the commonest cause of Venus flytrap death is prodding the traps to watch them close.

Most carnivorous plants require bright light, and most will look better under such conditions, as this encourages them to synthesise red and purple anthocyanin pigments. Nepenthes and Pinguicula will do better out of full sun, but most other species are happy in direct sunlight.

Carnivores mostly live in bogs, and those that do not are generally tropical. Hence, most require high humidity. On a small scale, this can be achieved by placing the plant in a wide saucer containing pebbles that are kept permanently wet. Small Nepenthes species grow well in large terraria.

Many carnivores are temperate, and although most are intolerant of hard frosts, many can be kept outside in temperate climates for the majority of the year. The main exception to this are Nepenthes sp., which are tropical, and require temperatures from 20 to 30°C to thrive.

Carnivorous plants mostly live in bogs, and require appropriate nutrient-poor soil. Most appreciate a 3:1 mixture of Sphagnum peat to sharp sand (coir is an acceptable, and more ecofriendly substitute for peat). Nepenthes will grow in orchid compost, or in pure Sphagnum moss.

Ironically, carnivorous plants are themselves susceptible to infestation by parasites such as aphids or mealybugs. Although small infestations can be removed by hand, larger infestations necessitate use of an insecticide. Isopropyl alcohol (rubbing alcohol) is effective as a topical insecticide. Diazinon is an excellent systemic insecticide that is tolerated by most carnivorous plants. Malathion and Acephate (Orthene) have also been reported as tolerable by carnivorous plants.

Although insects can be a problem, by far the biggest killer of carnivorous plants (besides human maltreatment) is grey mould (Botrytis cinerea). This thrives under warm, humid conditions, and can be a real problem in winter. To some extent, temperate carnivorous plants can be protected from this pathogen by ensuring that they are kept cool in winter, and that any dead leaves are removed promptly. If this fails, a fungicide is in order.

The easiest carnivorous plants for beginners are those from the cool temperate zone. These plants will do well under cool greenhouse conditions (minimum 5°C in winter, maximum 25°C in summer) if kept in wide trays of acidified or rain water during summer, and kept moist during winter:

• Drosera capensis, the Cape sundew: attractive strap-leaved sundew, pink flowers, very tolerant of maltreatment.
• Drosera binata, the fork-leaved sundew: large, Y-shaped leaves.
• Sarracenia flava, the yellow trumpet pitcher: yellow, attractively veined leaves, yellow flowers in spring.
• Pingicula grandiflora, the common butterwort: beautiful lilac flowers in spring, hibernates as a bud (hibernaculum) in winter. Fully hardy.
• Pingicula moranensis, the Mexican butterwort: pink flowers, non-carnivorous leaves in winter.
• Darlingtonia californica, the cobra lily: dramatic leaves, purple and lime-green flowers, likes to be watered with large amounts of cooled water during summer.

Venus flytraps will do well under these conditions, but is actually rather difficult to grow: even if treated well, it will often succumb to grey mould in winter unless well ventilated. Some of the lowland Nepenthes are very easy to grow, as long as they are provided with relatively constant, hot and humid conditions.

Pop culture

A fanciful carnivorous plant with an insatiable appetite was the central theme of the comedic play, Little Shop of Horrors, made from a more serious 1960s movie of the same name.

The triffids presented in John Wyndham's book The Day of the Triffids are plants which can uproot themselves, move, and can kill with a poisonous, whip-like tail. The book leaves open the question of whether the triffids are intelligent.

The film Attack of the Killer Tomatoes is a campy movie about tomatoes that for some reason eat people. It is an intentional spoof on 50s monster movies.

A large floral plant consumed a young woman in Madagascar in 1878, as witnessed by Dr Carl Liche, or so he reported in the September 26 1920 issue of The American Weekly. The woman was supposed to have been a member of the Mkodos, a little known but cruel tribe. The woman was pictured in an accompanying artwork. In 1925 the same paper offered another carnivorous plant story, of a tree species on Mindanao, in the Philippines. There is no evidence that either of these plants is more than a fanciful story.

References

• Juniper, B. E. et al (1989) The carnivorous plants. Academic Press Limited.

• Givnish, T. J., Burkhardt, E. L., Happel, R. E. & Weintraub, J. D. (1984). Carnivory in the bromeliad Brocchinia reducta, with a cost-benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. American Naturalist 124 479-497.

• Brewer, J. S. (1999). Effects of competition, litter, and disturbance on an annual carnivorous plant (Utricularia juncea). Plant Ecology 140 159-165.

• Thoren, L. M. & Karlsson, P. S. (1998). Effects of supplementary feeding on growth and reproduction of three carnivorous plant species in a subarctic environment. Journal of Ecology 86 501-510.

• Zamora, R., Gomez, J. M. & Hodar, J. A. (1998). Fitness responses of a carnivorous plant in contrasting ecological scenarios. Ecology 79 1630-1644.

• Gallie, D. R. & Chang, S. C. (1997). Signal transduction in the carnivorous plant Sarracenia purpurea - regulation of secretory hydrolase expression during development and in response to resources Plant Physiology 115 1461-1471.

• Zamora, R., Gomez, & J. M. Hodar, J. A. (1997). Responses of a carnivorous plant to prey and inorganic nutrients in a Mediterranean environment. Oecologia 111 443-451.

• Hanslin, H. M. & Karlsson, P. S. (1996). Nitrogen uptake from prey and substrate as affected by prey capture level and plant reproductive status in four carnivorous plant species. Oecologia 106 370-375.

• Deridder, F. & Dhondt, A. A. (1992). A positive correlation between naturally captured prey, growth and flowering in Drosera intermedia in two contrasting habitats. Belgian Journal of Botany 125 33-40.

• Knight, S. E. & Frost, T. M. (1991). Bladder control in Utricularia macrorhiza - lake-specific variation in plant investment in carnivory. Ecology 72 728-734.

External links

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• The Carnivorous Plant FAQ (http://www.sarracenia.com/faq.html)
• Carnivorous Plant discussion forum (http://terraforums.com/)
• Carnivorous Plant Database (http://www.omnisterra.com/bot/cp_home.cgi), provides an up to date, searchable database of all the published species of carnivorous plant
• Carnivorous Plant Nurseries (http://www.paonline.com/mrmiller/Nurseries.htm)
• The Carnivorous Plant Society (http://www.thecarnivorousplantsociety.org/), has a 24/7 live link with a forum.
• The Carnivorous Plant Society (http://www.thecps.org.uk/), the UK Carnivorous Plant Society has information on carnivorous plants and tips on cultivation.
• International Carnivorous Plant Society (http://www.carnivorousplants.org/), provides an extensive FAQ and links to the Carnivorous Plant Web Ring.
• Insectivorous Plants (http://pages.britishlibrary.net/charles.darwin3/insectivorous/insect01.htm), by Charles Darwin.
• Givnish paper on modelling carnivory (http://www.jstor.org/view/00030147/di006263/00p0048e/0), requires JSTOR subscription.
• International carnivorous plant society (http://www.carnivorousplants.org/cpn/samples/Science262Evol.htm), discussion of relationships within the Caryophyllales.