Classification - Carnivorous Plant by Makoto Honda

Carnivorous Plants Website

Carnivorous Plants in the Wilderness

by Makoto Honda

Carnivorous Plants
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I. Anatomy of Carnivory
2017-03-15
Updated 2020-11-12

FOR CARNIVORY TO TAKE EFFECT, there must be contact between leaf and prey. If a fly alights on a leaf and a moment later flies away, the contact is not sufficient. A fly must be persuaded to stay for a period during which the digestion can take place.

The first step in the sequence of events leading to successful carnivory is a lure that brings prey to physical proximity. Capture follows (forced detention). Digestion then starts that decomposes the prey. The digestion proceeds with plant's own enzyme or with the help of other commensal organisms. Finally, absorption takes place that carries the products of digestion into the leaf and to the growth site of the plant.

(1) Lure --> (2) Capture --> (3) Digestion --> (4) Absorption

The main nutrients selectively absorbed by carnivorous plants are nitrogen (N) and phosphorus (P) -- major plant nutrients -- but some other elements required in trace amounts such as potassium (K: kalium) and magnesium (Mg) are also utilized by some species.

Trap Mechanism There are four major trap types used by carnivorous plants: Pitfall trap, adhesive trap, snap-trap, and suction trap (with another somewhat related lobster-pot trap). We tend to emphasize the trap mechanisms when we analyze relatedness of different carnivorous plants, but digestion/absorption schemes that they use are just as significant in their evolutionary pathway.

Glands A gland is a structure which secretes fluids. Normally the walls of the epidermal cells are covered with a cuticle to reduce water loss, but the outer cells of a gland have a thin, perforated cuticle. Glands play a significant role in carnivory: Glands are used for lure (nectaries - nectar glands), digestion (enzyme secretion) and absorption of the digestion products. For adhesive traps, the glands are also used to secrete viscous mucilage (or resin in the case of Roridula). Depending on the types of traps, different kinds of glands perform different functions, or the same gland assumes multiple tasks.

Digestion In pitfall traps, the digestion can start in the preformulated fluids immediately upon prey capture. In other trap types, there is detection/perception of stimuli associated with prey capture, and the digestive process is initiated within a certain time frame. The absorption of the products of digestion is usually carried out by the same digestive glands. In the case of some traps that do not possess any glands for absorption, cuticular discontinuities provide passage of nutrients into the leaf tissue.

Repeatability Generally, adhesive secretion repeats many times, but may occur only once, as in Pinguicula’s adhesive glands. Likewise, the secretion of digestive enzyme may repeat several times, as in Dionaea, or can occur only once, as in Pinguicula, depending on the gland anatomy (presence or absence of conducting tissues to the gland).

EVOLUTION

CARNIVOROUS PLANTS (CP) EMERGED FROM non-carnivores at several distinct points in evolution. They only appeared as either a pitfall or adhesive trap -- and then, only some adhesives moved on to more sophisticated trap mechanisms.

CP emerged as pitfalls in:
           ----- In the order Ericales:
           Darlingtonia / Sarracenia / Heliamphora
           ----- In the order Oxalidales:
           Cephalotus

CP emerged as adhesive traps in:
           ----- In the order Caryophyllales:
           Drosera >> Snap-traps (Aldrovanda / Dionaea)
                            >> Pitfall (Nepenthes) >> Adhesive again (Drosophyllum >>Triphyophyllum)
           ----- In the order Lamiales:
           Pinguicula >> Lobster pot (Genlisea) >> Suction trap (Utricularia)
           Ibicella / Proboscidea --- x
           Byblis --- x
           Philcoxia --- x
           ----- In the order Ericales:
           Roridula --- x

           (* Molecular systematics places Roridula and Sarraceniaceae in the same Ericales order and they are closely related.
               While Roridula is adhesive (resin) and Sarracenia/Darlingtonia/Heliamphora are pitfall, both families share a very
               similar absorption mechanism - the efficient absorption of the prey-derived nutrients is achieved by the cuticular
               discontinuity of the leaf surface.)

Aquatic Environment Pushed Evolution

In sundews (order Caryophyllales) and butterworts (order Lamiales), both of which are adhesive carnivores, the transition to aquatic environment seems to have exerted pressure to move forward to more sophisticated trapping schemes (provided we assume Drosera-Aldrovanda-Dionaea evolution order).

Movement in Capture

We note that in the course of adaptation to carnivory, there are two distinct points at which physical movement was acquired during prey capture, leading to so-called "active" traps in carnivorous plants. One is in the order Caryophyllales in the branch leading to Drosera -- namely the Drosera's tentacle bending (and leaf folding) that eventually led to the snap-traps of Aldrovanda and Dionaea. In the same order, the branch leading to Nepenthes, Drosophyllum and Triphyophyllum either lost or did not acquire any such movement. The other is the leaf movement (curling and dishing) in Pinguicula upon prey capture that --- though not as direct or obvious a transition as in Droseraceae --- may have some connection to the workings of some aspect of Utricularia traps...
Some comments on use of the term "active" : The active trap simply means some movement is visible to the naked eye. If water molecules move in the trap, it is not visible. So, a bladderwort trap may be considered passive -- until it blasts as a result of gradual expulsion of water. The distinction between "active" and "passive" traps may be somewhat artificial...

REF: PLANT MOVEMENT IN RESPONSE TO STIMULI

1) Nastic Movement - movement in a pre-determined direction, regardless of the location of stimuli.

2) Tropistic Movement - movement in a direction that has correlation to the direction/location of stimuli.

    Phototropism - movement toward light
    Gravitropism - movement in response to gravity
    Thigmotropism - movement in response to physical touch

Occurrences of Sticky Carnivores

We often talk about the number of occurrences of carnivory in the course of angiosperm (flowering plant) evolution. In the order Lamiales, there appears to be multiple, independent points at which adhesive-trap carnivores emerged (Philcoxia, Byblis, Ibicella/Proboscidea, Pinguicula). But there are many non-carnivorous taxa in this order that possess glandular foliage, generally for defense purpose. These adhesive glands probably can be traced back to a very ancient common origin. Given what we do not know, once a reasonably efficient and workable gland structure has been established, creating a sticky carnivore out of a sticky defense seems a relatively small step. Therefore, even if this final step toward carnivory might have been undertaken independently in a handful of different families in Lamiales, considering these occurrences completely independent is a little misleading (or of little value). We should be cognizant of the fact that carnivory requires a lot of things and the ground work had started long ago, probably in the common ancestors of these families. This certainly does not suggest to imply that "carnivory" had been contemplated upon as a long-term goal when the gland structures were being developed eons ago and, from that point forward, having been worked on to finally come to fruition by this final step --- Evolution, by definition, does not have any "future" plan. What I am saying is that, once we understand what carnivory entails and how it might have come about, counting the number of occurrences of carnivory --- by just noting the final stage toward carnivory --- may not be as meaningful an endeavor as we might have initially thought.

“Sticky" Difference

There are many adhesive-trap carnivores that use sticky mucus to capture prey. They are found in three orders: Caryophyllales, Ericales and Lamiales. It is interesting to note that all adhesive glands of carnivorous plants are stalked glands raised above the leaf surface by some length; none of them are sessile glands (stalkless).

Darwin noted some difference between Drosera and Drosophyllum in their mucilage characteristics. In order to highlight this subtle but crucial difference, let us divide sticky-leaf carnivores into two groups. Drosera is the only member in Group 1, and the rest goes to Group 2. This grouping has to do with the way the digestive process is carried out after prey are captured by the adhesive glands.

DUAL-ABILITY OF STALKED GLANDS

Among all sticky-leaf glands, Drosera’s stalked glands (tentacles) are the only glands that have acquired the "dual" ability to perform digestive process (secreting digestive enzymes and absorbing the products of digestion) in addition to prey capture. In all the others, digestion is carried out by separate sessile glands scattered on the leaf surface. This means, for all these carnivorous plants in Group 2, keeping the trapped prey high on the tip of the stalked glands is meaningless, for no digestion will take place there --- the prey must be dropped down on the leaf surface. As noted by some observers (including Darwin), the Drosophyllum’s glue tends to peel off from the gland upon prey capture, exactly for this reason. This is in contrast to the Drosera’s glue that typically remains on the tentacle head to hold the prey during and after prey capture.

By and large, similar trapping behavior can be observed in all adhesive traps belonging to Group 2. In Pinguicula, for instance, the stalked glands readily collapse upon prey capture. This will allow the prey to sink down to the leaf surface and touch the sessile glands. That said, physical contact between prey and digestive glands may not be necessary for digestive process, so long as the small gap between them is bridged with fluids: For digestion, secreted fluids rich with enzyme must touch the body of the prey; for absorption, the fluids containing the digestion products must reach the absorptive glands. Keeping prey on the tall stalked glands of Drosophyllum is not likely to achieve this.

STALKED GLAND MORPHOLOGY
As mentioned above, the mucilage tends to peel off from the gland upon prey capture in Group 2 carnivores. There may be some difference in mucilage chemical composition that explains this behavior. Comparing the shape of glands in Group 1 & 2, the gland morphology also seems to support the difference in this behavior...

Group 1 (Drosera) --- The entire, spherical surface of the gland secretes sticky mucilage (i.e., the entire surface has cuticular gaps). As a result of this, the mucilage covers the entire gland surface in sundew tentacles. The contact area between mucilage and gland tends to be large, and therefore the mucilage is more securely attached to the gland.

Group 2 (Drosophyllum, Triphyophyllum, and Pinguicula) --- The gland itself at the stalk tip is flat-shaped, and only the upper surface of the gland secretes mucilage. As such, the mucilage tends to sit on a dish-shaped gland, rather than covering the entire gland. This small contact area may account for the easier detachability of the mucilage from the gland upon prey capture in Drosophyllum.

CLASSIFICATION OF CARNIVOROUS PLANTS / CP PHYLOGENY

CARNIVORY AT A GLANCE
(illustration) ------------ under construction

FOR VARIOUS CP GENERA BELOW, we present the anatomy of carnivory in four steps showing the basic mechanisms involved.

(1) LURE
- visual (leaf color / leaf shape / dewy-look... UV absorption pattern)
- olfactory (fragrance)
- food (nectar)

(2) CAPTURE
- pitfall trap (pitcher-shaped leaf / waxy surface / slippery hairs / retentive hairs...)
- adhesive trap (adhesive glands - how many times)
- snap-trap (aquatic waterwheel plant / terrestrial Venus flytrap)
- lobster-pot trap (glands – water flow / hairs)
- suction trap (glands – water expulsion)

(3) DIGESTION
- enzyme secretion by digestive glands - the Golgi apparatus (stimuli detection / how many times...)
- commensals (bacteria / commensal organisms / inquilines)