Carnivorous plants

Huntsman's cup.
Sarracenia purpurea, the purple huntsman's cup, showing the tradeoff between efficient survival (traps) and efficient reproduction (flowers).

When plants kill

All plants need nitrogen and phosphorus to build proteins and nucleic acids. Most plants get these elements from the soil, where they are released by bacteria and fungi during the breakdown of dead matter. However, in some habitats the growth of these micro-organisms is suppressed and the soil becomes impoverished. These conditions are found in blanket peat bogs, where the growth of the moss Sphagnum produces organic acids, which kills many of the microbes that usually recycle nutrients in the soil. This is made worse by the high rainfall in such areas, which tends to leach out nitrate anions from the soil, to which they are not tightly bound. Similar problems face some epiphytes (plants that grow on other plants, like air-plants), because there is very little soil to extract nitrates or phosphates from on the branches of a tree. Some plants living under these conditions have solved the problem by forming symbioses with nitrogen-fixing bacteria. However, carnivorous plants have evolved to steal the nitrates and phosphates of animals, which have become their prey. However, carnivory comes with a cost - that of producing the traps required to efficiently catch and use animal protein. For carnivory to be favoured by natural selection, the benefits of enhanced growth and reproductive success (due to better nutrition) must outweigh these costs.

How do plants become carnivorous?

There are over a quarter of a million species of flowering plant, but of these, only around five hundred and fifty are known to be carnivorous. True carnivory has probably evolved about ten times. Some of these 'independent' groups are probably descended from a recent common ancestor with a predisposition to carnivory, an ancestor that has also produced non-carnivorous descendants. For example, the Droseraceae, Nepenthaceae, Triphyophyllum and Drosophyllum are all closely related within in the Caryophyllales, and probably had a recent common ancestor with a predisposition (preadaptation) to carnivory such as mucilage-secreting glands. These groups form a clade with families such as the Polygonaceae, Plumbaginaceae, Tamaricaceae and Ancistrocladaceae, many of which have either salt- or mucilage-secreting glands on their leaves or calyces. As a result, this group contains both carnivorous, quasi-carnivorous and non-carnivorous descendants. The groups that have more-or-less independently evolved true carnivory are listed below:

  1. Lamiales
    • Lentibulariaceae. Three very distinct traps from one common ancestor: Pinguicula (butterwort) is a flypaper, Utricularia (bladderwort) is a bladder trap and Genlisea (corkscrew plant) is a lobster pot.
    • Byblis. The rainbow plant, another flypaper. May be closely allied to the Lentibulariaceae.
  2. Caryophyllales
    • Nepenthaceae. The tropical pitcher plants or monkey cups (Nepenthes).
    • Droseraceae. Drosera (sundews) are flypapers, Dionaea (Venus flytrap) and Aldrovanda (waterwheel plant, a sort of underwater Venus flytrap) are snaptraps.
    • Drosophyllaceae. Just one species, Drosophyllum lusitanicum, the dewy pine, a passive flypaper. Closely related to Triphyophyllum, and less closely related to the Droseraceae.
    • Dioncophyllaceae. Several non-carnivorous genera, plus Triphyophyllum peltatum. Flypaper, only carnivorous just before flowering.
  3. Ericales
    • Sarraceniaceae. American pitcher plants. Sarracenia are the trumpet pitchers, Heliamphora are the marsh pitchers, from the tepuis mountains of Amazonia, and Darlingtonia is the cobra lily. Related to the heathers.
    • Roridula, two not-quite-carnivorous plants which catch insects for a symbiotic assassin bug. Allied with the Sarraceniaceae.
  4. Oxalidaceae. Single carnivore (Cephalotus follicularis) amongst many other non-carnivorous species. Albany pitcher plant.
  5. Bromeliaceae. Many sub-carnivorous species, but only two likely carnivores: Brocchinia reducta, a probable urn trap in the pineapple family, and Catopsis berteroniana, an arguable urn trap.

It has been suggested that all of the various trap types described below are modifications of a similar basic design - the glandular leaf. Glandular and even just hairy leaves have the ability to catch and retain drops of rainwater (especially if shield-shaped) in which bacteria can breed. Insects that land on the leaf can become held down 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-carnivores. Plants that were better at retaining insects or water therefore had a selective advantage, because they had access to more nutrients than plants less efficient at it. Rainwater can be retained better by cupping the leaf, leading to pitfall traps. Alternatively, insects can be retained by making the leaf stickier by the production of stickier mucilage, leading to flypaper traps.

Marsh pitcher.
Heliamphora nutans has simpler pitchers, which can be seen quite clearly to be rolled leaves.

Pitcher traps and derivatives

A good example here is seen in the three genera of the Sarraceniaceae. Pitcher traps are probably produced by cupping of a water-retaining (hairy?) leaf, followed by "zipping up" of the margins of the leaf and subsequent loss of most of the hairs, except at the bottom, where they help retain prey.

Yellow trumpet pitcher.
Sarracenia flava 'Maxima', a large and attractive American pitcher plant.

In Sarracenia, an operculum (lid) helps to stop the pitcher from overflowing with rain-water. These plants also have a battery of digestive enzymes to aid the bacterial action in the tube of the pitcher.

Cobra plant.
Darlingtonia californica, the cobra plant.

In Darlingtonia, the operculum grows entirely over the opening of the pitcher, and outgrowths from its tip form 'fangs' which serve as highways for ants and other arthropods. The balloon-like operculum also has translucent patches (areolae) to confuse prey inside, and prevent them from finding their way back out.

The lobsterpot traps of Genlisea (the corkscrew plant) and bladder traps of the bladderworts, Utricularia, may be modified pitchers that have adapted to aquatic prey, somewhat like Sarracenia psittacina does today. A flooded trap can be easily swum out of, so in Utricularia, a one way door has developed, turning a pitcher into a bladder-trap. This trap is in fact active: a partial vacuum inside the bladder is released by prey brushing against trigger hairs stuck to the door of the bladder, and this sucks prey inwards. In Genlisea, the trap is Y-shaped, and the opening to the lobster-pot is twisted along its lengths. The twist is an adaptation that displays as much trapping surface as possible in all directions when buried in moss. Hairs inside the traps force prey to move towards a digestive organ at the base of the modified leaf.

The carnivorous bromeliads, like Brocchinia and Catopsis have a quite different form of pitfall trap. 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.

Portuguese sundew.
Drosophyllum lusitanicum is a passive flypaper.

Flypaper traps and derivatives

A good example here is seen in three genera of the Caryophyllales. 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 could have evolved.

Alice sundew.
Drosera aliciae is an active flypaper: prey are trapped by mucilage, but slow movement of the leaf ensures that more prey items are retained despite their struggles.

The active flypaper traps require a little more explanation. Rapid plant movement can be due to actual rapid growth (thigmotropism), or it can be due to rapid changes in cell turgor (thigmonasty), which allow cells to expand or contract by quickly altering their water content. Slow flypaper traps like Pinguicula and Drosera use growth.

Venus flytrap.
Dionaea muscipula is an snap-trap: prey are trapped by rapid plant movements.

Faster 'flypaper' traps, like the Venus flytrap, use 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 are now the teeth and trigger hairs - an example of natural selection hijacking preexisting structures for entirely new functions.

Evolution of the carnivorous syndrome is almost trivially simple: many plants are probably accidentally carnivorous anyway, by virtue of having water-retaining leaves. It may only take a small selection pressure for obtaining extra nitrogen and phosphorus from sources other than the soil to push the plant on its way to carnivory, by small improvements of 'design':

  1. A way to retain struggling prey (wax, hairs, glue, cupping).
  2. A way to attract more prey (nectar, colouration, scent).
  3. A way to deal with prey more effectively (encourage bacterial decay, or maggots, or secrete enzymes).
  4. An increase the efficiency of foliar feeding (absorbative glands).
  5. Fine tuning, like the production of overhanging teeth, insecticides, movement and false escape holes.

Carnivory is an adaptation, and like anything else produced by natural selection, it is the combination of thousands of small changes over long periods of time, each change contributing a little to the survival of its possessor. Carnivory has evolved a number of times, so it seems unlikely to be a very difficult adaptation to acquire, so why aren't there more species exploiting animals in this way? In particular, why are there only a few carnivorous bromeliads, when their ready-made insect drowning urns make them such obvious candidates?

Carnivorous habitats

The best way to begin answering this question is to study the habitats where the plants are found. The archetypal carnivore, the Venus flytrap, has to put up with quite extreme environmental conditions. It grows in soil where the soil nitrate and calcium levels are almost too low to measure. This poses an obvious problem to growth 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 encourages the production of toxic ions such as ammonium, and its pH is an extremely acidic 4. 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 kill.

Pygmy sundew.
Drosera pygmaea is a pygmy sundew that is quite unable to use soil borne nitrate.

However, on the plus side, the habitat is warm, very sunny, constantly moist, and the plant experiences relatively little competition from low growing Sphagnum moss, amongst others. This sort of habitat is typical of many carnivorous plants, and carnivores have a reputation as bog plants. However, they are also found in very atypical habitats too. For example, Drosophyllum lusitanicum is found around desert edges. So why are carnivores so often restricted to wet, soggy, sunny sites, and how can they 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 (rarely) potassium, when the usual sources in the soil are very low. However, there is a spectrum of dependency on prey. Pygmy sundews are unable to use nitrate from soil because they lack the necessary enzymes, so they are almost entirely dependent on animal prey. Common butterworts (Pinguicula vulgaris) on the other hand can use inorganic sources of nitrogen (soil) better than organic ones (animals), but a mixture of both gives better growth than either alone. European bladderworts seem able to use either source equally well. So animal prey makes up for deficiencies in soil nutrients, but to different extents in different plants.

Modelling carnivory

In the normal course of things, plants use their leaves to intercept sunlight. The light energy is reacted with carbon dioxide taken from the air and water from the soil, to make sugar (and other chemicals), and a waste product, oxygen. The sum total of all the sugars, amino acids, fats, etc., in the plant is called biomass. The accumulation of biomass is what the growth of the plant depends on, and this production of biomass from sunlight is called 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 "exhaust".

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, run out of energy, and die. Respiration and photosynthesis are very much the opposites of one another. Photosynthesis uses (light) energy and CO2 to make biomass and oxygen exhaust. Respiration burns biomass with oxygen to make (chemical) energy and CO2 exhaust. 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 respiring. This can be measured in the laboratory by seeing how much carbon dioxide a plant takes up (if it takes up CO2, it must be photosynthesising more than it is respiring).

In carnivorous plants, the leaf is not just used to photosynthesise, it is also used as a trap. The problem with this is that changing the leaf shape to make it a better trap makes it less efficient at photosynthesis. For example, pitchers have to be held upright, so that only their lids directly intercept light. Even worse, the plant 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. So, a carnivorous plant will have both decreased photosynthesis and increased respiration, making the potential for growth small. Those were the expenses, so what about the returns of carnivory? These are the nitrogen and phosphorus, harvested from the corpses, and essential for the growth of all living things. 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 having enormous amounts of a nitrogen rich enzyme called Rubisco (short for ribulose-1,5-bis-phosphate carboxylase/oxygenase), which is the most abundant protein on Earth. So, the returns of carnivory, should be more efficient photosynthesis.

Clearly some sort of tradeoff will occur. It is intuitively obvious that the Venus flytrap is 'more carnivorous' than Triphyophyllum peltatum: the first 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 answer is probably yes, but there doesn't seem to be any obvious scale of carnivory that we can use. But, there is! We can use the energy 'wasted' by the plant in building and fuelling its trap.

The respiration of a plant increases as it become more carnivorous, but (up to a point) so too does its photosynthesis as nutrients become less limiting. Hence there will be an optimum carnivory at some finite, measurable value.
In a zero nutrient habitat, photosynthesis cannot occur without carnivory. However, massive expenditure in carnivorous adaptations is also penalised because eventually extra nutrients stop bringing benefits, as light or some other factor is in shorter supply than they are. Hence there is an optimum carnivory.

That is, we can measure carnivory as the respiration of the plant due to making and maintaining carnivorous structures. This allows us to plot a graph that models the behaviour of the leaf of a carnivorous plant. Above is a graph of carbon dioxide uptake (potential for growth) against trap respiration (carnivory) for a leaf in a sunny habitat containing no soil nutrients at all. Respiration is a straight (green) line sloping down under the horizontal axis, because respiration produces carbon dioxide. The line is straight because we are actually defining carnivorous-ness as carnivory-related respiration. Gross photosynthesis is a curved (blue) line above the axis: as carnivorous-ness increases, so too does the photosynthesis of the trap, because the leaf is receiving a better supply of nitrogen and phosphorus. However, this payoff doesn't last forever. Eventually some other factor (such as light intensity) will become more limiting to photosynthesis than nitrogen or phosphorus supply: if you make a cake, you can buy as much flour as you want, but it'll be no use at all if you don't have any gas to cook it with. As a result, increasing the carnivory of the leaf will not make the plant grow any better: you would have to increase the light harvesting efficiency instead. When you add the two lines together you get the red line. This represents the net uptake of carbon dioxide, and therefore the plant's potential for growth. As I said earlier, this must be positive for the plant to survive. There is a broad span of carnivory where this is true, and there is also an optimum. Plants with a carnivory 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, and natural selection will weed them out, leaving the better-adapted optimal plants behind. At zero carnivory 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.

In a habitat where nutrients are not limiting, there is very little increase in photosynthesis as carnivory increases. Hence the optimum carnivory will be very close to zero.
In a nutrient rich habitat, growth at zero carnivory can occur. However, this is also the optimum carnivory for a plant, as any investment in traps reduces net photosynthesis (growth) to less than the net photosynthesis of a non-carnivorous plant. In comparison, in a habitat with lots of soil nutrients but little light, the gross photosynthesis curve will be lower and flatter, because light will be more limiting than nutrients. When we add up the curves this time, the optimum carnivory is at zero. So the optimum amount of energy to use in building and maintaining your trap is none. Carnivorous plants exist between these two extremes.

Evidence

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.

In general, carnivorous plants are poor competitors, because they invest 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: carnivores are to nutrients what cactuses are to water. Carnivory only seems to pay off when the nutrient stress is very high and light is abundant. When these conditions are not met, some plants give up carnivory temporarily. If you grow carnivorous plants, you'll know that trumpet pitchers produce flat, non-carnivorous leaves (phyllodes) in winter. Light levels are lower than in summer, so light is more limiting than nutrients, and carnivory doesn't pay. The lack of insects in winter exacerbates the problem. Also, if you damage very small pitcher leaves, they will be unable to form proper pitchers, and 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 butterworts and the Albany pitcher plant in the less favourable seasons. Part-time carnivory in Triphyophyllum peltatum may be due to an unusually high need for nutrients just before flowering. Some carnivores can adjust their carnivory to suit their habitat: Utricularia vulgaris can sense the nutrient content of the water it is growing in. You might expect that in low nutrient water, the plant would produce more traps, because the payoff would be greater. Strangely, it actually produces more traps in nutrient rich water. It is probably using the nutrients in the water as a cue that the water contains lots of phytoplankton, and hence lots of prey too.

The more carnivorous a plant is, the more conventional you would expect its habitat 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 more typical for non-carnivores). Drosophyllum comes from arid areas, and is a passive flypapers, which is probably the lowest maintenance trap you can get. Energy conservation is the name of the game: pitcher plants frequently skimp on enzyme production compared to traps that have intermittent prey capture (like the Venus flytrap) because they can rely on bacteria to do their digestion for them. Venus flytraps are also very choosy about the size of prey they digest, which is filtered by the teeth around the trap's edge, so that energy is not wasted on prey 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.

Why so few?

The answer to this question is that 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 squandering your hard earned biomass on frivolities like trigger hairs and enzymes worthwhile. Many plants occasionally benefit from animal protein rotting on their leaves, but carnivory obvious enough for us to notice and pigeonhole it is rarely worth the effort.

And why so few bromeliads? Most bromeliads are epiphytes, and most epiphytes grow in partial shade on tree branches (Nepenthes at least has the option to climb up a tree to the light). It is noteworthy that two of the known carnivorous bromeliads are ground dwellers. 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 dingy for more extreme, more recognisable carnivory to evolve. A frequent definition of a carnivore is a plant that attracts, captures, kills, digests, absorbs, and benefits from animal prey. Fulfilling all these criteria to become a fully-fledged carnivore is a pretty tall order, so what constitutes a carnivore depends pretty much on how stringent your definition is. Obviously therefore, so too does their rarity.

Bibliography

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