On the lack of succulence in leguminous plants, with a side-note on Bignoniaceae

There are some factual errors which are problematic, and some missing lesser known species.

Firstly, the Leguminosae or Fabaceae (depending on what you call it) is a single monophyletic family, consisting now of 6 subfamilies according to LPWG 2017. The Mimosoids are imbedded within the Caesalpinoids and thus a new classification was proposed.

There are other Indigofera that could be considered as succulent, but you first need to quantify what is succulence.

"A species of Senna in South America is said to have somewhat succulent photosynthetic stems, but not leaves".
Maybe referring to:
https://www.inaturalist.org/taxa/324277-Senna-crassiramea
https://www.inaturalist.org/taxa/484147-Senna-aphylla
https://www.inaturalist.org/taxa/983596-Senna-pachyrrhiza

Continuing from above, there is this other similar Senna in South America:
https://www.inaturalist.org/taxa/1235413-Senna-spiniflora

In California and Nevada, this Senna has only very tiny leaflets:
https://www.inaturalist.org/taxa/79057-Senna-armata
https://www.inaturalist.org/observations/112915169

The following is the email I sent, immediately after reading of the discovery of Oberholzeria etendekaensis: 

From: Antoni
Sent: Tuesday, March 01, 2016 11:17 AM
To: wessel@kaokosafari.com
Subject: congratulations on describing the first succulent-leafed leguminous plant on Earth
 
Dear Wessel Swanepoel,
 
It was with great interest that I read your recent (2015) article describing Oberholzeria etendekaensis.
 
I have been aware for several decades that the leguminous families, although extremely diverse ecologically and in growth-form, lack succulence in their foliage. I have been on the lookout for exceptions, but until your discovery I found nothing more than a few species in Psoralea, Aspalathus and Indigofera in littoral situations in the Western Cape, where the leaves are fleshy owing to saline aerosol (a common syndrome affecting many families of plants that grow in the littoral zone, and presumably representing a facultative rather than obligate fleshiness in the leguminous species).
 
So, as far as I can see, your Oberholzeria is unique globally: an obligately succulent member of the Fabaceae sensu lato.
 
I’ve been thinking about why leguminous plants seem so resolutely lacking in succulence of the xerophytic type. Here are a few hypotheses.
 
Leguminous plants, in general, specialise in augmenting nitrogen. Some, such as most Papilionoideae, do this with rhizobial nodules on their roots, but others do it with ectomycorrhizae (the typical syndrome in miombo trees). Although southern Africa has a remarkably diversity, at the family level, of succulent plants, I know of few – if any – of the succulent species that fix nitrogen or have particular adaptations to augment nitrogen. So there seems to be, in general, a pattern of mutual exclusion between succulence and N-augmentation and the virtually complete lack (except for Oberholzeria) of succulence in leguminous plants seems consistent with this pattern.
 
Secondly, leguminous plants, in general, seem to specialise in emphasis of the ‘stalks’ within the leaf, i.e. the rachis and petiole. The pinnate or bipinnate leaf, so typical of leguminous plants, represents a kind of multiplication of the leaf-stalk structures, whereas – at the opposite end of the spectrum – the phyllode represents a loss of everything except the petiole, which is expanded into a photosynthetic surface in its own right. But what links a bipinnately compound leaf with a mere phyllode is the extreme evolution of the fibrous framework/support structure of the leaf, something de-emphasised in the xerophytic succulent syndrome. What I’ve noticed is that, despite the manifold origins of succulent plants by convergent evolution, there seems to be no species of succulent, worldwide, that has a succulent petiole as the main form of foliage, or that has succulence in a truly pinnate leaf with more than three pinnae (Kalanchoe of the Crassulaceae may perhaps be a kind of exception?). Your Oberholzia pushes the limits in the sense that it manages to have succulent pinnae in the trifoliolate leaf, which makes it even more exceptional. That is to say, if you told me that you had discovered a succulent leguminous plant and asked me to guess the leaf-form, I would have guessed a simple leaf, not a compound leaf. Oberholzeria is, in this sense, a double surprise: not only a succulent leguminous plant but also one with a truly pinnate (albeit with a minimal number of pinnae) leaf.
 
I would predict that Oberholzeria lacks any mechanism for fixing nitrogen, and indeed I would go further by predicting that it lacks even the vesicular-arbuscular mycorrhizae so common in both herbaceous and woody plants. There are not that many non-mycorrhizal plants on Earth but, as I understand it, succulent plants do include non-mycorrhizal species and it seems to me that succulence tends to be a growth-form with little to gain from microbial or fungal nutritional symbioses.
 
Anyway, these are just some hastily jotted-down thoughts in excitement at your discovery. Your discovery deserves to be widely appreciated. I’d love to hear your thoughts in terms of a biological interpretation of this plant.
 
With many thanks,
Sincerely,
Dr Antoni V. Milewski
Percy FitzPatrick Institute

The difference in the incidence of succulence (of the xerophytic type) is among the most important ecological differences between Australia and southern Africa, and deserves to be recognised more widely than is currently the case.

It is not just that succulents are abundant and widespread in southern Africa. It is also that there is a remarkable variety of succulent growth forms and physiological strategies there.

As one example, Portulacaria afra (https://www.inaturalist.org/taxa/326086-Portulacaria-afra) deviates from the usual pattern that succulents grow slowly, because it somehow manages to combine crassulacean acid metabolism with rapid growth.
 
Why does Australia have so few succulents, whereas southern Africa has so many?
 
I would exclude halophytes, because they just confuse the picture. Minus the halophytes, the ‘succulent’ flora of Australia can be seen for what it is: extremely limited, to the degree that only a few taxa qualify, and no vegetation type contains succulents as more than a minor contributor to cover. The few Australian succulents are mainly Sarcozona (https://www.inaturalist.org/observations?place_id=any&taxon_id=624242&view=species) and Roepera aurantiaca (https://www.inaturalist.org/observations?taxon_id=778973), a genus shared with southern Africa.

A complication here is that we would have to consider Carpobrotus (https://www.inaturalist.org/observations?place_id=any&taxon_id=49323&view=species) carefully on a species-by-species basis, to decide whether they are halophytic or not.
 
The main explanation is climatic and pyric, with soil nutrient regimes playing a subordinate role.
 
Succulence generally goes with shallow roots (often also lacking mycorrhizae), and succulents tend to occur in climates that combine overall semi-aridity with relatively frequent precipitation (not necessarily rain). So the succulent karroo (https://en.wikipedia.org/wiki/Succulent_Karoo) in southern Africa tends to be associated with advection fog, which has no counterpart in semi-arid Australia.
 
A climatic explanation for Portulacaria afra, which is a succulent large shrub dominating patches of vegetation in the Eastern Cape (https://en.wikipedia.org/wiki/Eastern_Cape), has little to do with fog or mist, and here a more complicated explanation must be sought, involving soil nutrients and mega-herbivory. However, it is noteworthy that parts of the Eastern Cape have bimodal rainfall, a pattern poorly represented in the corresponding eastern half of Australia.
 
Fire regimes are crucial for explaining the intercontinental difference. This is because few succulents persist in any fire regime, although there are some short-lived perennial mesembs in South Africa that contribute to a seral stage in semi-arid fynbos, which does burn. Even the halophytic succulents in Australia tend to be restricted to landforms that are either fire-free or have fire so occasionally that no plant in these communities is adapted to fire.

I invoke this observation, in part, to explain another anomaly of Australian biogeography, namely the absence of land tortoises.

Land tortoises, like succulent plants, are particularly vulnerable to fire. This means that the only land tortoises on Earth that live in fire-prone habitats (e.g. pine savannas in Florida, plus some forms of fynbos in South Africa) tend to depend on refuges such as deep burrows or rocky outcrops. In Australia the only possible refuges would be burrows, which I rationalise would be physiologically punishing in saline soils.
 
A reason why vast areas of southern Africa lack fire regimes is that the vegetation there was so much more heavily browsed and grazed by large animals. So, according to this rationale, the abundance of elephant, rhinos, equids, and many forms of ruminants in southern Africa was part of the regime favouring foliage-succulence. The epitome of this is the vegetation dominated by Portulacaria afra. However, the pattern is, I suggest, widespread in southern Africa.
 
Potassium as such does not have much explanatory power for succulent foliage, although it does have major explanatory power for succulent fruits, worldwide. This is because potassium is a cheap and mobile element, and a major basis for the rationale in the case of succulent fruits is continual flow of large amounts of potassium through the plants. Of course it does take potassium to maintain succulence in foliage, but the green parts of succulent plants are long-lasting, minimising losses of potassium.

Fleshy cylindrical phyllodes: Acacia pinguifolia
Fleshy cylindrical leaflets: Senna artemisioides ssp. filifolia