International Carnivorous Plant Society

Evolution of the Oxalidales Carnivore

Cephalotus follicularis

Cephalotus follicularis. Photo © Richard Nunn.

 

Until the advent of molecular phylogeny, plant taxonomists had no clue where Cephalotus follicularis fits into the tree of life. The most common guesses were that it was related to Sarracenia and Nepenthes (as if they are related!) or to the Saxifragales where Drosera was once thought to reside.

Thanks to DNA sequencing we now know Cephalotus is in the order Oxalidales (oxalis) and not related to any other carnivorous plant. It ties in at the root of the Oxalidales and has as sisters 5 families with over 1900 species in 60 genera, most of which you have never heard of. The family Cephalotaceae has one genus with one species. For what it is worth, the closest outgroup orders are the Cucurbitales (cucumber, begonia) and Fagales (beech, walnut, and she-oak). For Cephalotus does a family tree like that fit the definition of orphan?

 

Oxalidales phylogeny

Genetic relationships of the plant families in the order Oxalidales based on two chloroplast (rbcL, matK) sequences and one mitochondria (matR) DNA sequence from the NCBI taxonomy database. The sequence data do not provide adequate resolution to show additional hierarchy. That means none of these families in the Oxalidales appear to be closer to Cephalotus than any other. The display order of the branches is arbitrary. I put them in this order because the leaf structure of the Oxalidaceae and Connaraceae is similar to the Cephalotus ancestral leaf structure. (Whether the family Huaceae should also be in the Oxalidales is debatable and not shown in the tree.)

 

There are indications from fossils and models of molecular clocks that the split among the families of the Oxalidales occurred 80 to 100 million years ago. If the progenitors of all these families became distinct within a ten million year period 100 million years ago, there may be no way to sort out the relationships better than this. That is because there would be so few preserved DNA changes during that short period compared to number of changes since then.

The number of genera and species listed in the figure to some extent is a matter of opinion, but the numbers and geographic range give a good idea of the size and diversity of the families related to Cephalotus. Four of the six families are found in Southwest Australia where Cephalotus is found. The Elaeocarpaceae, Cunoniaceae, Brunelliaceae, and Connaraceae are generally evergreen shrubs. The Oxalidaceae consists mostly of herbaceous plants in the genus Oxalis but the family also contains some shrubs and small trees in other genera.

 

Cephalotus Flowers

Cephalotus follicularis flowers. Notice the flowers have 6 tepals, 6 pistils, and 12 alternately shorter stamens. The flowers are about 10 mm wide. Oxalis flowers are similar but typically have 5 sepals, 5 petals, 5 pistils, and 10 alternately shorter stamens.

 

Within the order Oxalidales, the Oxalidaceae and Connaraceae have compound leaves. The species in the other families tend to have simple leaves. The same mixed situation exists in the related outgroup orders. Leaf structure says more about the environment where the plants are found than their heritage. The same goes for flowers. Plant/pollinator interactions determine large scale aspects of flowers such as petals and colors. Cephalotus appears to have ancestral-like flowers and it may have the same pollinators it had 80 million years ago. Some of its relatives appear to also have ancestral-like flowers. That does not mean those relatives are the nearest relatives. 

There has been a long discussion in the literature about how the pitchers of Cephalotus are constructed. Plant anatomists have been staring at and slicing and dicing the pitchers since the middle of the 19th century. On a general inspection the pitchers are as elaborate as any Nepenthes pitcher. But more detailed inspection showed that the pitchers are not your folded simple leaf like with Sarracenia and Nepenthes. Lloyd (1942) and DeGreef (1990 PDF) summarize the studies demonstrating this and discuss the results under the assumption Cephalotus is a member of the Saxifragales and proto-Cephalotus had a peltate saxifrage-type leaf.

 

Stem veins

Left: Cross section of a Cephalotus leaf petiole showing the circular arrangement of vascular bundles. The flat side of the petiole is the lid side. Right: Cross section is of an Oxalis triangularis leaf petiole. This is typical of peltate leaves. Notice how the Oxalis triangularis has five bundles while Cephalotus has six. This mirrors the situation with the flowers.

 

Evidence that Cephalotus is derived from a peltate leaf is the arrangement of vascular bundles in the petiole. In a typical simple or flat leaf the bundles are arranged in an arc. In Cephalotus they are arranged in a circle exactly like Oxalis leaves except Oxalis has one fewer bundle. Curiously you can also take an Oxalis leaf and easily fold it into a pitcher. With a little stretching, the lid would be one leaflet. The leaf ridges that act as prey guides would be at the sutures between the leaflets.

 

Developing Pitcher

Two views of a developing Cephalotus pitcher. The pitcher is a severely modified, Oxalis-like compound peltate leaf. The three "prey guides", one on the front and one on each side of the pitcher, are leaflet sutures. There are also leaflet sutures between the side back segments and the lid segment although they are not as prominent. It is possible the front guide is actually two sutures with a leaf remnant in between. With the front prey guide being a leaf remnant, that makes six leaflet segments. Six segments would also match the number and position of the vascular bundles in the petiole.

 

These physically superficial similarities but basic differences between Oxalis and Cephalotus are consistent with them being in separate but related families as shown by the DNA sequences. It is not possible to determine what the common ancestor looked like because all the other families in the Oxalidales have simple leaves. Eighty million years is plenty of time for the progenitors of Cephalotus to develop their own compound peltate leaf style and then have that evolve into a pitcher.

 

Cephalotus follicularis

Cephalotus follicularis with large non-carnivorous leaves. Photo © Richard Nunn.

 

Probably the biggest impediment for some people to understand Cephalotus pitchers is the simple, non-carnivorous leaves the plant produces seasonally. DeGreef points out these leaves are unifacial phylodes rather than normal bifacial leaves. They are essentially expanded petioles and extremely unlikely to be representative of ancestral leaves. The simple leaves are produced during the winter when presumably there are not enough prey available to make production of pitchers advantageous. They also tend to be more common on shade grown plants. The occasional aberrant leaves we see more than likely happen when the development pathway to produce pitchers kicks in after the leaf has started to grow and it is too late for that leaf to make proper pitchers. The structure of the aberrant leaves is totally consistent with the peltate nature of the trapping leaves and an ancestor with Oxalis-like leaves.

-- John Brittnacher
March 2011
Latest update January 2020

 

For a more detailed discussion please see the following articles and articles they reference.

Keep in mind each author states their view at a given time with the data they have at that time. Recent discoveries could modify their ideas.

 

DeGreef, John D. (1990) Cephalotus follicularis: history and evolution. Carniv. Pl. Newslett. 19(3-4):95-103 ( PDF )

Lloyd, Francis E. (1942) The Carnivorous Plants. Chronica Botanica, Waltham MA, USA. (reprinted by Lloyd Press).

Mann, Phill (2005) Observations on Cephalotus follicularis and Drosera binata in Western Australia. Carniv. Pl. Newslett. 34(3):68-70 ( PDF )

Stevens, P. F. (2001 onwards). Oxalidales. IN: Angiosperm Phylogeny Website. Version 14, July 2017 [and more or less continuously updated since].

Cross, Adam, Nick Kalfas, Richard Nunn and John Conran (2019) Cephalotus - the Albany Pitcher Plant. Redfern Natural History Productions, Poole, Dorset, England.

 

Cephalotus

Cephalotus follicularis.

Cephalotus pitcher

Longitudinal section through a Cephalotus trap.

Oxalis leaf

Oxalis leaf, an example of a compound peltate leaf consisting of three leaflets. I consider it peltate because all of the leaflets are equally terminal. Photo by Tom Cahill.

Cephalotus sprout

Cephalotus sprout showing a unifacial phylodia as the first true leaf and a pitcher as the second true leaf. This aspect may be variable.

abberant pitcher

Aberrant Cephalotus leaf. Photo by RL7836.

Cephalotus leaf

Aberrant unifacial winter leaf.

Cephalotus leaf

Aberrant unifacial winter leaf.