The Evolution of Carnivorous Plants
Some of the most bizarre and fascinating plants in the natural world are undoubtedly carnivorous plants. Carnivory, defined as the consumption of animal tissue, is often only associated with the animal kingdom. However the existence of carnivory is widespread and diverse in the plant and fungi kingdoms as well. Specifically carnivorous plants, which originally descended from exclusively photosynthetic plants, have evolved elaborate, efficient, and diverse methods to capture, digest, and metabolize passing insects and microorganisms.
Since Darwin’s landmark work Insectivorous plants, observers of carnivorous plants have tried to answer fundamental questions regarding their nature. Why would an exclusively photosynthetic plant expend valuable developmental resources to form structures for carnivory? How do these plants capture prey and why do they do it? This paper will explore characteristics, nature, and physiology of carnivorous plants as well as several possible reasons and methods for the evolution of carnivory in plants. Carnivorous plants are members of the in the angiosperm family (flowering plants).
As the most diverse division of land plants, angiosperms have developed full carnivory six times in their phylogeny. There are approximately 600 species of carnivorous plants, representing eleven families and nineteen genera of angiosperms (Huebl et al. , 2006). Carnivorous plants are widely distributed across the globe and can be found on all continents except for Antarctica. They are generally found in bog and fen conditions or any other habitat where the soil is very low in nutrients, slightly acidic, and or hypoxic (Academac, 1997).
The most basic definition of carnivory in plants is the ability to absorb the products of decomposed organisms, either directly on the leaves or through roots in the soil, to increase nutrient absorption which ultimately increases seed production and overall fitness. While this definition includes most exclusively photosynthetic plants (pure autotrophs), a more specific definition of carnivorous plants is that they should have at least the ability to attract, capture, and digest their prey, which are typically arthropods or protozoans (Chase et al. , 2010).
It should be noted that there is a distinction between parasitic and carnivorous plants. Carnivorous plants are classified as photoheterotrophs, or organisms that depend on both light for photosynthesis and organic carbon from prey. Parasitic plants require a host plant to survive and draw nutrients from. While all trap structures of carnivorous plants are highly specialized leaves, each group is distinguished by the specific specialization of the leaf. The three primary categories of carnivorous plants, separated by capture method, are active traps, semi-active traps, and passive traps.
These categories are refined further as plants are classified as either snap, pitfall, flypaper, bladder, or lobster-pot traps. The most dramatic and sinister of all carnivorous plants are active traps. Two widely recognized examples of active snap traps are Dionaea muscipula, the Venus Fly Trap, and Aldrovanda vesiculosa, the Water Wheel. Active traps most often use touch-sensitive hairs that trigger the plant’s capture mechanism when stimulated. For instance, the trap structures of the Venus Fly Trap are two broad, jaw-like leaves which form a symmetrical clamshell.
The leaves are lined with interlocking spines around the edges and are held open at about 45° to 60°. When a prey insect touches a trigger hair, the trap will only close if another trigger hair is stimulated within approximately twenty seconds (Hodick & Sievers, 1988). This double action-potential requirement prevents the trap from wasting energy by closing unnecessarily due to random stimuli from objects the plant cannot digest. Dionaea muscipula is one of the fastest moving touch-sensitive plant species in the world, closing as quickly as 500 ms once a prey insect has touched a trigger hair twice.
The explanation of this lightning closure is in a rapid change in the turgidity of the cells. This means that there is a sudden change in the water pressure in the cells at the seam between the two trap leaves, which causes a group of specialized cells, called mesophyll cells, to expand (Hodick & Sievers, 1988). Once viable, organic prey is captured, the trap clamps down further to form a tight, sealed pouch around the organism. Enzymes are secreted from glands on the inside of the trap surface and the prey is digested in approximately ten days. Passive traps are less agile than active traps but just as lethally efficient.
An example of a passive pitfall trap is Heliamphora, or the sun pitcher plant. Pitfall traps are deep cylinders with open tops and liquid, usually a mixture of digestive enzymes and water, pooled at the bottom. The prey climbs into the pitcher and becomes trapped in the sticky liquid in the bottom. It is prevented from climbing back up the side walls due to tiny downward-pointing spines and is digested by either enzymes created by the plant or by bacteria washed in from the outside. Insects are often lured by bright colors and the emission of volatiles that resemble compounds found in fruit.
This is an instance of mimicry in which the carnivorous plant has evolved to mimic fruit in order to attract insects or other animal prey (Jurgens et al. , 2009). Passive traps also include flypaper traps such as Pinguicula, the butterwort. These plants have sticky mucilage surfaces on their leaves that lure insects by imitating moisture. Once the prey is stuck to the leaf surface, struggling triggers a secondary set of glands, the sessile glands, to secrete digestive enzymes. The enzymes break down the digestible components of the insect body into smaller compounds which can be absorbed through pores in the surface of the leaf.
Some species of Pinguicula have the ability to slightly bend their leaves in response to physical stimuli, allowing them to grip prey. An example of a semi-active trap would be Ultricularia, or the bladderwort. The aquatic bladderwort uses osmosis to create a vacuum in each of its small, bladder traps. Before the trigger hairs are brushed by prey, each of the bladders is deflated as a result of vacuum pressure. When trigger hairs are stimulated, a trapdoor opens, the bladder inflates, and the organism is sucked inside where it is digested. The final type of passive trap is the lobster-pot trap.
Lobster-pot traps are deep, labyrinthine chambers that are easy to enter but difficult or impossible to exit. The funnel shaped leaves in Genlisea, the corkscrew plant, form spiraling tubes that ultimately lead to the plants utricle, or digestion chamber. The inside of the tubes are lined inward pointing hairs that only allow the prey to enter and move downwards towards the utricle. Plants most often evolve carnivory to supplement nutrient absorption. Carnivorous plants are usually found in bog and swamp-like environments with acidic, waterlogged, and nutrient poor soil.
These soils are also abundant with decomposing plant matter. The decomposing organic matter leads to high concentrations of acidic H2S, which in turn lowers reduction-oxidation potentials. Low redox potentials solubilize metals such as iron and manganese, creating toxic soil conditions for plant roots (Academac, 1997). While most carnivorous plants are photosynthetic and able to use CO2 from the air like any other autotroph, they are partially dependent on nitrogen and organic carbon from capture organisms due to poor soil conditions (Academec, 1997). A study on Pinguicula vulgaris revealed hat enriching the soil of the plant led to 100% biomass increase while feeding the plant extra insects only yielded 25%. However, through combination of both methods, feeding and soil enrichment, increased biomass by almost 200% (Academac, 1997). This shows that the roots of carnivorous plants are more than capable of fully absorbing any nutrients in the soil and are only dependent on trapping mechanisms because of poor soil conditions. The ultimate goal of evolving carnivorous structures for plants in less than ideal habitats is to increase survival and reproductive fitness.
There are three identified benefits to evolving carnivory that directly increase the plant’s overall fitness. First, by capturing and digesting prey, plants can increase photosynthesis. Plants with limited access to sunlight would benefit from enhanced photosynthesis afforded by carnivory. Second, nutrients from carnivory increase the quality and quantity of seed production. Thirdly, aquatic carnivorous plants can get organic carbon directly from prey instead of depending on photosynthesis (Ellison & Gotelli, 2009).
On the other hand, the cost of carnivory is that growing extra carnivorous structures requires precious developmental energy. A study placed Pinguicula vallisneriifolia, a fly paper trap, in shady conditions. The plant reduced its mucilage production to avoid allocating its limited carbon to costly carnivorous structures. It has also been shown that when a carnivorous plant is supplied with additional nutrients via the soil, it will reduce developmental resources to its trap structures because obtaining nutrients through root uptake is less costly (Ellison & Gotelli, 2009).
While carnivory has evolved independently six times in four different angiosperm orders, carnivorous plants often exhibit very close morphological convergence of their structures and methods of capturing prey (Ellison, 2006). This theory of independent origins of carnivorous plants (the similarities in structure brought about by convergent evolution) was first proposed by Darwin in Insectivorous plants (1875). The opposing theory, that all carnivorous plants are from a single lineage and appeared near the base of the angiosperm lineage, was offered by Croziat (1960).
Most recently, examination of relationships between families of carnivorous plants (Ellison & Gotelli, 2008). The problem with studying the evolution of carnivorous plants is that they are very poorly represented in the fossil record. They produce very few leaves and the soft trap structures do not fossilize. Therefore the only methods to map the possible evolutionary pathways carnivorous plants might have followed are to analyze DNA sequences and examine similarities among living specimens. There are two current theories on the evolution of carnivorous plants. The first is the ‘energetics hypothesis’.
This hypothesis asserts that rapid morphological evolution results from a single or small number of changes in regulatory genes which control plant functions that strive to meet the high energy demands of active traps. For example, the relaxed morphological requirements of its aquatic habitat, high mutation rates, and a few changes in key regulatory genes could be the driving force in the diversity of Utricularia (Ellison & Gotelli, 2009). The ‘predictable prey capture hypothesis’ suggests that complex traps tend to capture more prey in predictable ways and the more efficient the trap is, the more morphologically diverse it will become.
The reasoning for this hypothesis is that carnivorous plants are able to utilize “biosynthetic building blocks, such as amino acids, peptides, and nucleotides” from digested prey. These building blocks are attributed to rapid morphological evolution. Highly specialized traps such as Utricularia and Genlisea are extremely efficient and tend to have the most prey captures relative to other types of carnivorous plants, therefore the theory contends that there is a direct relationship between the number of prey captures and morphological evolution.
By evaluating data on the rate and mode of evolution, prey capture methods, and the costs and benefits of expending energy in developing structures for carnivory in plants, researchers concluded that the evidence better supports the energetics hypothesis (Ellison & Gotelli, 2009). Active snap traps have the ability to catch larger prey than simple sticky traps. This means that if the ability to capture larger prey was selected for, then prehensile snap traps could have evolved from passive sticky traps with adhesive surfaces (Gibson et al. 2009). A proposed evolutionary pathway of carnivorous plants is that these plants evolved sticky glandular surfaces as defense against insects and desiccation. The secretion of mucilage enabled these proto-carnivorous plants the mechanism of “defensive predation”. This means that the glands often caught or killed insects they ensnared in defense but the plant did not actually digest the organisms. These glands eventually evolved to secrete enzymes and absorb nutrients.
Now that the plants were able to digest the insects they captured, they began to evolve bright pigments and olfactory stimuli, attracting insects by mimicking fruit. With the advent of vascularized glands, these surfaces began to react to physical and chemical stimuli. Combined with the action-potential of trigger hairs, this enables leaf bending to grip and trap prey, as exhibited in Droseracae, Dionaea muscipula, and Aldrovanda vesiculosa (Huebl et al. , 2006).
Therefore it is possible to theorize that carnivorous plants, or at least one of the six lineages of carnivorous plants, diversified from this simple adaptation and evolved many different specialized trapping methods. Along the Droseracae lineage, an active trap family which is characterized by leaf movement, Nepenthaceae, the pitcher plants, could have diverged later when the glands began secreting digestive enzymes and absorbing nutrients. Drosophyllacae, a passive flypaper trap family, may have diverged at the point when the glands became vascularized.
Moreover, the most specialized and active traps, such as Dionea muscipula and Utricularia, have evolved more recently than simpler passive traps, like Pinguicula and Nepenthaceae. Some plants, such as Ancistrocladus, have even developed and lost carnivory along their evolutionary history (Huebl et al. , 2006). This may have occurred due to changing environmental factors or slow migration out of poor soil conditions where it would become too costly to develop extra carnivorous structures.
In summary, carnivorous plants are a diverse group of plants from the angiosperm order. Carnivory in plants, defined as the ability to capture and digest animals, has evolved independently multiple times in order for plants to adapt to new habitats with less-than-optimal soil conditions. Carnivorous plants can access nutrients through prey capture and become less dependent on optimal soil and light conditions. Small mutations in regulatory genes under the right conditions could allow plants to evolve proto-carnivorous structures and eventually, full scale carnivory.
Differing degrees of carnivory and the diversity of trap mechanisms, ranging from active to passive traps, reveal that certain modern carnivorous plants could descend from the same lineage, diverging in character along their evolutionary pathway. Our understanding of these innovative plants has come a long way since Darwin’s Insectivorous plants. But while they are certainly some of the most intriguing and critically studied of all angiosperms, there is still much to learn about the evolutionary history of carnivorous plants. Resources Adamec, L. 1997.
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