Carnivorous Plant Diversity and Evolution: Part 1 – An introduction to Killer Plants

Figure 1.          A photograph showing part of my own carnivorous plant collection taken in September 2017. From left to right: Sarracenia sp. (likely a hybrid of S. leucophylla), S. flava, S. purpurea purpurea, S. minor, Sarracenia x ‘Maroon’, S. psittacina, Sarracenia x ‘Maroon’, Dionaea muscipula. Photograph by Julian Kiely. 

Hello all,

Welcome to Palaeoflora, and to my first blog post! I already have many ideas of articles I’d like to write, however, to begin with I wanted to cover a topic which I have a particular interest in, and is very dear to me; Carnivorous Plants! Many people are aware of the existence of carnivorous plants, but this knowledge often extends only to the famous Venus Fly-Trap (Dionaea muscipula), with the Pitcher Plants of Asia and America (Nepenthes and Sarracenia respectively) coming a close second. But the diversity of modern carnivorous plants in both morphology and taxonomy is truly astounding, and even within the course of researching for this article, I discovered many more lineages of carnivorous, or possibly carnivorous plants than I even suspected. In this first article I will provide an introduction to carnivorous plants, their habitats and their various trapping mechanisms. In the second article I would like to take you on a guided tour of modern carnivorous plant diversity, and describe to you the biology of the various carnivorous plants which exist today. And in my third article I will be focusing on the evolution, phylogeny and fossil record of carnivorous plants, and will also talk about speculations which can be made about their inclusion within prehistoric environments and palaeoart. So, without further ado, I’ll begin our journey, through the world of Carnivorous Plants!

So, what are these so called ‘Carnivorous Plants’?

There are two main terms used to describe carnivorous plants; the first is of course ‘carnivorous’ and the second is ‘insectivorous’. Throughout this blog I have chosen to refer to them by the former name, as while it is true that most carnivorous plants prey primarily upon insects, many will also trap other animals (including vertebrates on occasion). Next, when we say ‘carnivorous plant’ what do we actually mean? Well, The Kew Plant Glossary (Second Edition, Beentje 2016) provides the following definition:

‘carnivorous, plants that trap animals and derive some or most of their minerals from digesting them’

While this provides us with a basic definition for vegetable carnivory, I would like to suggest a few more criteria which most carnivorous plants adhere to:

• ·         They actively implement methods of attracting their prey to their traps.
• ·         They must permanently trap their prey, causing their eventual death. 
• ·         They utilise methods of breaking down their prey to extract minerals from them.
• ·         And finally, they must be able to absorb those minerals either directly or indirectly from their prey.

However, even these criteria are not present in all ‘carnivores’ (in these cases I may be inclined to use the term ‘pseudocarnivory’), and even within true carnivores there are some which are active and some which are passive. Active and passive can also have several meanings; in the case of water filled pitfall traps, ‘active carnivory’ indicates that the plant produces its own digestive enzymes, and ‘passive carnivory’ indicates the presence of symbiotic bacteria, which aids in digestion. However, ‘active carnivory’ can also be used to mean a trap which responds to stimuli from its prey with movement, and a ‘passive carnivore’ is one which does not.  So, as you can see, the division between what is and what isn’t carnivorous is not as finely cut as most people think, but instead more of a blur. All levels and stages of carnivory are present in modern floras, from plants which display perhaps only one carnivorous feature, to those who are fully carnivorous.

Figure 2.         A Simplified evolutionary tree of carnivorous plants, showing all modern genera which are considered to be ‘true carnivores’ (however, both Roridula and Byblis are not technically true carnivores, I have included them here as they are often included in discussions about carnivorous plants). The thumbnails show the basic trap design of each genus, and the darker green indicates the evolution of carnivory within a clade, and the light green indicates their non-carnivorous ancestors. As you can see, carnivory has evolved independently at least eight times within plants (although some authors may include up to ten, Ellison and Adamec, 2018, while others identify only six, Ellison and Gotelli, 2008). This tree is based primarily on Ellison and Gotelli, 2008, with updates from Ellison and Adamec, 2018. Artwork by Julian Kiely.

Fantastic Carnivores and Where to Find Them

Within modern carnivorous plants, of which there are over 600 extant species (Ellison and Gotelli, 2008; Christenhusz, Fay and Chase 2017), there are many different forms of trapping mechanisms, which often have evolved independently in multiple lineages; it is thought that full, true carnivory has evolved independently in at least six modern lineages (Ellison and Gotelli, 2008), all of which are angiosperms (so, unfortunately no known carnivorous ferns – yet…) (see Figure 2.). The convergent evolution of carnivory multiple times within plants indicates that there must be some big advantages to having it, but under what sort of conditions does it occur? Well, in modern carnivorous plants, carnivory is a way for the plants to acquire minerals vital for their growth, and this is often most useful when they grow in environments with very low mineral content. These habitats are often very wet and sometimes permanently waterlogged, as in these habitats the presence of water leaches minerals out of the substrate (soil), creating low concentrations of the minerals which plants require to grow. For this reason, many carnivorous plants can be found growing in peat bogs and semi-aquatic environments, around the world, and even here in the British Isles (where I live) there are ten species of carnivorous plants across three genera (Rose and O’Reillyn 2006) (see Figure 3.).

This may also be a good time to dispel the myth that carnivorous plants are all tropical and require warm temperatures; while it is true that some carnivorous plants do live in the tropics, many are also found in temperate regions across the globe. Sarracenia, the North American Trumpet Pitchers are found as far north as Canada and Alaska, and can survive frost and being frozen for short periods of time (USD Plant Database; D’Amato 2013; Christenhusz, Fay and Chase 2017). There is even a species of Pinguicula (Pinguicula alpina, the Alpine Butterwort) which is found in Siberia and Iceland, and in mountain ranges across Eurasia, were it thrives in the cold conditions (Slack 1979). 

Figure 3.         A photograph showing two of our native carnivorous plant species, Pinguicula vulgaris and Drosera rotundifolia. I found these growing primarily in sphagnum moss or on bare rocks, on well-watered valley slopes in Snowdonia. In cultivation, it is generally advised, particularly for Pinguicula, not get too much water on the leaves, as this impairs their trapping ability; however, seeing them in the wild was interesting, as often they would be growing in the algae and slime covered rocks in pools of waters and slow flowing streams, often partially submerged. This indicates that in at least some species, wild individuals are able to grow quite happily in conditions which would generally be considered sub-optimum in cultivation. Photograph taken by Julian Kiely, July 2017.

Rainy, wet and humid environments are often common places for carnivorous plants to evolve, because these conditions make the production of aqueous substances, such as the nectar-like ‘glue’ of many flypaper traps, a worthwhile investment; in these conditions, the virtually unlimited supply of water allows the production of large quantities of aqueous substances, and the humidity prevents these substances from evaporating quickly (Ellison and Adamec, 2018). An exception to this association of carnivorous plants with water is Drosophyllum (the Dewy Pine), which instead grows in the dry, nutrient poor, fire-prone sandstone soils of the Western Mediterranean (Ellison and Adamec, 2018). Epiphytic carnivorous plants are also known, however this is uncommon; among angiosperms as a whole, ~ 9% are epiphytes, whereas among carnivorous species, only 2% are, with many of these not representing true epiphytism, as they often inhabit wet microsites such as the water filled tanks of bromeliads.

           

Tricks and Traps of Carnivorous Plants  

  

Modern carnivorous Plants are incredibly diverse, and show many different methods of catching their prey, but despite their often independent origins the same forms of traps have evolved time and time again. In the past, this has led some scientists to classify certain species together, which have now been shown to be unrelated. A prime example of this is Roridulaceae, a monogeneric family containing the genus Roridula, which in the past has been associated with both Droseraceae and Byblidaceae (all three families are similar for containing genera which produce sticky flypaper traps), but is in fact a sister clade to Sarraceniaceae (the American Pitcher Plants) (Christenhusz, Fay and Chase 2017). 

Figure 4.         A basic diagram of the 17 modern genera of carnivorous plants, grouped by the type of traps they possess. Overlaps indicate where the genus contains species which display multiple forms of traps. Genera depicted, clockwise from top left: Utricularia, Aldrovanda, Dionaea, Drosera, Drosophyllum, Pinguicula, Byblis, Roridula, Triphyophyllum, Genlisea, Darlingtonia, Sarracenia, Nepenthes, Cephalotus, Heliamphora, Catopsis, Brocchinia. Artwork by Julian Kiely.

I have found that the various trapping mechanisms seen in modern carnivorous plants can be broadly classified into four different types; Flypaper Traps, Pitfall Traps, Motile Traps and Lobster-pot Traps (see Figure 4.).  

The most common form of trapping mechanism (the form which is present in the most modern genera) is the Pitfall Trap; these traps have evolved independently on 5 occasions (twice within Bromeliaceae, and once in the Nepenthales, Rosids and Ericales), and are generally composed of a single leaf which has developed into a funnel or pitcher-like shape which holds water (hence the common name pitcher plant). An exception to this are the carnivorous bromeliads, whose traps are composed of a rosette of tightly packed leaves, which holds water in the middle. As the bromeliad carnivores are very different in morphology from other pitfall traps, for the moment we will ignore them in this general description. In the eudicot pitfall traps (Figure 5.), most species possess a lid; these  are flat extensions of the leaf, which extend over the opening of the pitfall trap, and generally prevent the traps from flooding with too much rainwater, however many individual species have adapted the lid to perform a variety of other functions. The peristome (rim of the opening) varies greatly between different species, being not much more than a rolled edge in Sarracenia and often highly developed in Cephalotus and Nepenthes; it is often smooth with a slippery surface. The lid, neck and occasionally peristome of pitfall traps produce nectar, which is used to attract insect prey with the sugary liquid. Ultraviolet patterns which resemble those flowers use to direct pollinators are also present in some species (Ellison and Adamec, 2018). When the prey lands, they will often slip on the smooth, waxy surface of the peristome, and fall into the pitcher chamber of the trap, which is often water filled (this can be rain collected water as in Heliamphora, or self-secreted, as in Darlingtonia). The slippery inner walls and (often present) downward pointing hairs prevent the prey from climbing up to escape, and instead the prey drowns in the water. This water may contain digestive enzymes produced by the plant, or may rely upon symbiotic bacteria to digest their prey. Minerals are then absorbed by the plant via glands at the base of the pitcher chamber. Carnivorous bromeliads similarly utilise ultraviolet patterns and a slippery surface, but instead have adventitious roots growing into the water tank, which absorb minerals (Christenhusz, Fay and Chase 2017).

Figure 5.         Pitcher Plant cross-section, morphological comparison. From left to right, Nepenthes, Sarracenia, Cephalotus (not to scale). Ax, Leaf Apex; DZ, Digestive (glandular) Zone; Li, Lid; PC, Pitcher Chamber; Ps, Peristome; Te, Tendril; Wa, Water; Wi, Wing. By Julian Kiely.

             The second most common form of trap is the Flypaper Trap. These traps are often composed of leaves with glandular hairs which secrete a sticky substance at their tip. In addition to these secretory glands, many (but not all) flypaper traps also possess glands which produce digestive enzymes and absorb minerals from the digested prey. Flypaper traps are often designed to catch small flying insects, which are attracted to the leaves by the sparkling dew (sticky substance), which in some instances produce ultraviolet patterns similar to the markings of some flowers (Ellison and Adamec, 2018). Once the insect lands, the sticky ‘glue’ prevents them from escaping and, in most cases, suffocates the insects as the ‘glue’ clogs up their spiracles and trachea (tiny holes and tubes, along the sides of their body, which they use to breathe). At this point, some flypaper traps (such as those in Drosera) also act as motile traps, as their hairs and leaves fold inwards to wrap around the insect (Ellison and Adamec, 2018). The prey is then digested and the minerals adsorbed. Despite its seeming complexity, this is the simplest form of trap (with the possible exception of the pitfall traps of certain Poales).

Figure 6.         Drosera leaf life drawing and cross section. Ab, Abaxial leaf surface; DG, Digestive Glands; GH, Glandular Hair; Gu, ‘Glue’ (mucilage); TS, Trapping Surface. By Julian Kiely.

Motile traps are perhaps the most enigmatic of the carnivorous plants, and include the famous Venus Fly-Trap (Dionaea muscipula). The morphology of motile traps varies greatly between the handful of genera which have developed them, but the significant element in all of them it the use of movement to trap their prey. In some, such as Dionaea and Aldrovanda, they use two lobes of a leaf to snap shut around their prey when stimulated. As such these traps are sometimes referred to as ‘snap-traps’ (Ellison and Adamec, 2018). Another form of highly advanced motile trap is the bladder, or suction traps of Utricularia species, which grow on subterranean or aquatic stems where they are surrounded by water. Bladder traps are highly derived leaves which take the form of a hollow bladder with a trap door at one end. They work by pumping water out of the trap, creating a partial vacuum within them; when small prey stimulate hairs around the trapdoor, the trapdoor opens and the prey are sucked in. Once inside the trap, enzymes are released to break down the prey (Ellison and Adamec, 2018, Christenhusz, Fay and Chase 2017). As aforementioned, some Drosera and Pinguicula species also move in response to prey; in Pinguicula this movement is slow and minimal, but in Drosera it is often more rapid and noticeable (in D. glanduligera, the edges of their leaves possess snap-tentacles, which hinge inwards when stimulated, to further entrap prey; Ellison and Adamec, 2018). The lid Nepenthes gracilis also acts as a passive motile trap, utilising raindrops which hit the lid to throw prey into the pitcher (Ellison and Adamec, 2018).

Figure 7.         Dionaea muscipula life drawing and morphology diagram. DG, Digestive Glands; Lo, Lobes; MR, Midrib (hinge region); NG, Nectar Glands; Te, Teeth (cilia); TH, Trigger Hairs. By Julian Kiely.

The final form of trap is the lobster-pot trap (sometimes called a pigeon trap in Genlisea and Sarracenia psittacina). The basic mechanism of these traps is to have a one way entrance, so that the prey, once inside are unable to back out. In Darlingtonia (which is generally considered a pitfall trap) and S. psittacina, these traps are modified pitfall traps, where the lid and peristrome have fused and curved inwards (Figure 8.), to produce a small opening which funnels prey inwards, but prevents them from escaping back out of that opening. The pigeon trap, while similar in its trapping mechanism, is different in that it composes of a hollow tube with an opening at one end (in S. psittacina, the lobster-pot opening, and in Genlisea, small holes at intervals along the corkscrew like trap), and many stiff hairs within the tube pointing away from the opening. These hairs prevent any prey which enters the trap from moving backwards, so the prey moves slowly deeper and deeper into the trap before dying. Pigeon traps are generally submerged within water where, particularly in the case of S. psittacina, a standard pitfall trap would not work.

Figure 8.         Sarracenia psittacina cross section, morphology diagram. BPH, Backward Pointing Hairs; Li, Lid; LpT, Lobster-pot Trap; Ps, Peristome; PT, Pigeon Trap Region; Wi, Wing. By Julian Kiely.

              So, as you can see the diversity of trapping methods utilised by modern carnivorous plants is truly astounding, and reflects the many different prey items which they catch. There are many different deviations from the basic design of each trap and thus the above descriptions provide only the briefest of overviews. Carnivorous plants are so incredible and diverse that, even at the end of this series of blogs, I will have only scratched the surface of their biology and diversity. Next time I will introduce all the different genera of carnivorous (and possibly carnivorous) plants, talking more about the specific adaptations of each genus, and the species within each genus. I will also delve a little more into their basic phylogeny (although, this will be covered in more detail within Part 3).

But for now, I hope you have all enjoyed this blog and found it interesting and informative. As it is my first proper article I’m still getting used to the writing style, so I apologise if I have rambled a little bit. Please let me know what you have thought about it and whether there is anything I can improve on. I know some of you may feel cheated that in the first post on a palaeobotany blog there hasn’t been a single sign of a fossil, but trust me, I will be getting to that soon enough; so, if it helps, you could always think of this as just the preamble before the main show.

And with that, all that’s left to say is Thank-you Very Much for reading!

All the Best,

Julian Kiely

References

Beentji, H. (2016). The Kew Plant Glossary: an illustrated dictionary of plant terms. Second Edition. Kew Publishing, Royal Botanic Gardens, Kew.  

Christenhusz, M. J. M., Fay, M. F., Chase, M. W. (2017). Plants of the World, An Illustrated Encyclopaedia of Vascular Plants. Kew Publishing, Royal Botanic Gardens, Kew. 

D’Amato, P. (2013). The Savage Garden Revised. Second Edition. Ten Speed Press, Berkeley.

Ellison, A. M., Adamec, L. (2018). Carnivorous Plants: Physiology, Ecology, and Evolution. Oxford University Press, Great Clarendon Street, Oxford, OX2 6DP, United Kingdom.

Ellison, A. M., Gotelli, N. J. (2009). Energetics and the evolution of carnivorous plants—Darwin’s ‘most wonderful plants in the world’. Journal of Experimental Botany, Vol. 60, No. 1, pp. 19–42.

International Carnivorous Plant Society. Carnivorous Plant Trapping Mechanisms.  https://www.carnivorousplants.org/cp/carnivory/trapping

Rose, F., O’Reillyn, C. (2006). The Wild Flower Key: How to identify wild flowers, trees and shrubs in Britain and Ireland. Revised Edition. Penguin Books, 80 Strand, London, WC2R 0RL, England.

Slack, A. (1979). Carnivorous plants. Ebury Press, National Magazine House, 72 Broadwick Street, London, W1V 2BP.

Thorogood, C. J., Bauer, U., Hiscock, S. J. (2017). Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytologist, Vol. 217, pp. 1035 – 1041.

USD Plant Database. Sarracenia purpurea L.  purple pitcherplant. https://plants.usda.gov/core/profile?symbol=sapu4