Why does nodal-spinescent Ziziphus quadrilocularis dominate small areas of fire-free vegetation in Australia?

@russellcumming @marcoschmidtffm @stevemaldonadosilvestrini @shiwalee @tonyrebelo @danielcahen @ronf @s_k_johnsgard @andrew_hankey @richardgill @graham_g @troos @botaneek @dineshvalke

One of the unusual biogeographical features of Australia is the scarcity of spinescent, other than foliar-spinescent, plants.

Spines derived from stipules and stem-tips are abundant and diverse in Africa and tropical Asia, and certain biomes in the Americas. The plants bearing them, e.g. Vachellia (https://www.inaturalist.org/observations?place_id=any&taxon_id=72418&view=species), dominate vegetation over fairly extensive areas.

 By contrast, vegetation dominated by plants with spines - other than foliar spines - is so unusual in Australia that most naturalists will never have heard of examples.

There is a general correlation between the various forms of spinescence and fire regimes.

Vegetation dominated by foliar-spinescent species tends to be flammable, because these plants are pyrophytic (https://en.wikipedia.org/wiki/Pyrophyte). By contrast, vegetation dominated by nodal- or stem-spinescent species tends to be non-flammable, because the plants are 'pyrophobic', in adaptive terms.

In this Post, I point out an exception to the generalisation that nodal spinescence is scarce in Australia. Here is an intriguing biogeographical anomaly in the Australian flora.

My main sources are Beadle (The Vegetation of Australia, 1981, https://www.vgls.vic.gov.au/client/en_AU/VGLS-public/search/detailnonmodal?qu=Botany+--+Ecology.&d=ent%3A%2F%2FSD_ILS%2F0%2FSD_ILS%3A19930%7EILS%7E0&ps=300) and Beard (Vegetatio 31, 171-192, 1976).

Ziziphus (Rhamnaceae, https://www.inaturalist.org/observations?place_id=any&taxon_id=49042&view=species) is a largely tropical genus, containing about 40 spp. on several continents.

The plants are typically nodal-spinescent, i.e. the spines are stipular (https://www.inaturalist.org/observations/88540907 and https://www.inaturalist.org/observations/76110686). They are also somewhat drought-deciduous, and often subject to foraging by ungulates (https://pubmed.ncbi.nlm.nih.gov/14620591/ and https://link.springer.com/article/10.1007/s10722-007-9299-1), as well as caterpillars (https://www.asergeev.com/pictures/archives/compress/2015/1698/10x.htm).

Ziziphus produces fleshy fruits, which are dispersed and sown by a wide variety of vertebrates.

Certain species have been selectively bred to improve their fruits (https://www.researchgate.net/publication/291486321_Domestication_of_jujube_fruit_trees_Zizyphus_mauritiana_Lam and https://www.sciencedirect.com/science/article/abs/pii/S0304423819300494). Ziziphus jujuba (https://en.wikipedia.org/wiki/Jujube) has been so thoroughly domesticated that there are now more than 400 cultivars.

In subSaharan Africa, Ziziphus mucronata (https://www.inaturalist.org/taxa/340228-Ziziphus-mucronata) is widespread and well-known. However, it nowhere dominates vegetation, always being subordinate to acacias such as Vachellia spp.
 
Given the biogeographical pattern of this genus, it is no surprise that it extends to northern Australia.

However, what is surprising is that one species, namely Ziziphus quadrilocularis (https://en.wikipedia.org/wiki/Ziziphus_quadrilocularis), is restricted to Australia. (There are, as yet, no observations of this species in iNaturalist.)

Furthermore, Z. quadrilocularis actually dominates small areas of largely fire-free vegetation, in the Kimberley region (https://en.wikipedia.org/wiki/Kimberley_(Western_Australia)) of northernmost Western Australia. In this sense it actually outdoes its congener at similar latitudes in southern Africa, which fails to dominate even small patches of vegetation.

The vegetation in question in northern Australia is difficult to classify. However, it is listed under the heading of 'semi-evergreen vine forest' by Beadle (1981).
 
Ziziphus quadrilocularis, although occurring only in tropical climates, seems similar to other spp. in this genus in most ways. This includes nodal spinescence - albeit only in the ‘juvenile’ stage, which presumably means below a certain height above ground.

I do not know if this species shows recrudescence, in the sense that spines reappear above this height following damage to branches in the adult/mature crown.
 
Beadle (1981), page 181, describes rainforest-like vegetation in the Admiralty Gulf area (https://en.wikipedia.org/wiki/Admiralty_Gulf) of northernmost Western Australia, which occurs from near sea level to an altitude of about 250 m: “The low level forests are dominated by Ziziphus quadrilocularis”.

At higher altitudes within the same catena near Admiralty Gulf, Z. quadrilocularis is replaced by non-spinescent trees such as spp. of Albizia (https://www.inaturalist.org/observations?place_id=6744&taxon_id=47451&view=species), Atalaya (https://www.inaturalist.org/observations?place_id=any&taxon_id=184379&view=species), Cochlospermum (https://www.inaturalist.org/observations?place_id=any&taxon_id=132131&view=species), and Pouteria (https://www.inaturalist.org/observations?place_id=any&taxon_id=83117&view=species).
 
The situation with Ziziphus in Australia can be confusing. This is because

• there are at least two spp. of Ziziphus indigenous to Australia, plus at least one species recently introduced to the continent, and
• the introduded species, namely Ziziphus mauritiana (https://www.inaturalist.org/taxa/123697-Ziziphus-mauritiana), has a wide distribution, and is now sometimes regarded as an invasive weed (https://keyserver.lucidcentral.org/weeds/data/media/Html/ziziphus_mauritiana.htm and https://www.agric.wa.gov.au/declared-plants/chinee-apple-declared-pest).

Of the three spp. of Ziziphus in Australia, the only one I find biogeographically and ecologically remarkable is Z. quadrilocularis.

Ziziphus oenoplia (https://en.wikipedia.org/wiki/Ziziphus_oenoplia) has an unremarkable distribution, ranging from southern Asia into northern Australia. It seems typical of African-Asian spp. of Ziziphus, in its association with disturbance, and its ‘secondary growth’ following clearing of ‘climax’ vegetation. As far as I know, Z. oenoplia nowhere dominates vegetation in Australia.

As for Ziziphus mauritiana:
This is a typical tall shrub or low tree of the Indian jungles, as per Rudyard Kipling (see 'Setting' in https://en.wikipedia.org/wiki/The_Jungle_Book).

Indian jungles are

• anthropogenic rather than fully natural vegetation, consisting of indigenous shrubs, trees, and lianes that return rapidly after clearing, and may thus be termed ‘ruderal’ (https://en.wikipedia.org/wiki/Ruderal_species),
• thickets, similar to rainforests in being relatively free of wildfire, and lacking pyrophytes, and
• partially spinescent, consisting of relatively weedy woody plants, inadvertently selected by continual hacking, charcoal-making, medicine-collecting, honey-foraging, and other disturbance by the human species.

One of the reasons for the commonness of Z. mauritiana in the Indian jungles is that the fleshy fruits of this species (https://www.inaturalist.org/observations/103494560 and https://www.inaturalist.org/observations/88149225 and https://www.inaturalist.org/observations/70261271) are edible for the humans.
 
Adding to the complexity of the situation is that Z. mauritiana is partly a cultivated plant (‘ber’, https://specialtyproduce.com/produce/Ber_Indian_Jujube_11258.php). It is subject to selective breeding, as well as being a wild species.
 
Overall, Z. mauritiana is best-regarded as a ‘feral’, rather than fully wild, plant. And the Indian jungles to which it extends are anthropogenic and successional vegetation, not aptly described as 'rainforest’.

And so, Z. mauritiana in Australia cannot be considered an indigenous plant, let alone a wild one.

Because Z. quadrilocularis and Z. mauritiana are similar, the anthropogenic success of Z. mauritinana has tended to obscure the biogeographical and ecological anomaly posed by the Australian species.
 
Ziziphus quadrilocularis seems ecologically similar to Z. mauritiana, but is fully indigenous to Australia. So, in this sense, Australia seems, even before European arrival, to have had a ‘natural jungle’, complete with the nodal spinescence typical of ‘jungle’, at least over limited areas.

If so, was this related to disturbance by large animals? And, if so, which ones?
 
Given what seems to be a relatively ancient presence in the western part of the tropical zone of Australia, it is odd that Z. quadrilocularis is absent from Queensland (where there seems to have been no indigenous member of this genus). It would have surprised nobody to find that the only member restricted to Australasia is present in New Guinea or Timor (https://en.wikipedia.org/wiki/Timor). However, this is not the case.
 
The following show the distribution of Ziziphus quadrilocularis: https://bie.ala.org.au/species/https://id.biodiversity.org.au/node/apni/2889799 and https://florabase.dpaw.wa.gov.au/browse/profile/4848.

The part of the distribution with the most records, in the Kununurra-Lake Argyle-Timber Creek area (https://en.wikipedia.org/wiki/Lake_Argyle), seems not to contain any vegetation in which Z. quadrilocularis is particularly common. As a result, and because of confusion with Z. mauritiana, this fairly widespread species tends to be overlooked/underappreciated, over most of its range.

The following confirms that Ziziphus quadrilocularis, like its congeners, has stipular spines, which appear already in the seedling: https://apps.lucidcentral.org/rainforest/text/entities/ziziphus_quadrilocularis.htm. However, in Z. quadrilocuaris the spines are restricted to the ‘juvenile’ stage, in possible contrast to certain other spp. of Ziziphus that may retain stipular spines even in the adult/mature stage. I do not know if Z. quadrilocularis, like Z. mauritiana, has only one spine at each node.

Publicado el julio 23, 2022 09:50 TARDE por milewski