The mystery of the missing mycorrhizae

Everyone knows that the roots of most plants have an intimate mutualism with fungi, and that the invisible mycorrhizae formed in this way help plants to extract nutrients from soils (https://en.wikipedia.org/wiki/Mycorrhiza and https://mycorrhizas.info/ecm.html).

However, how many realise that some of these associations are more powerful than others, and that the most powerful mycorrhizae were naturally absent from regions where herbivores are naturally most abundant?

For example, one of the puzzles of global biogeography is that South Africa was virtually devoid of 'supermycorrhizae' common elsewhere in the world.

How did this come about?

Most mycorrhizal fungi have microscopic hyphae. However, ectotrophic mycorrhizae - or ectomycorrhizae for short - can be macroscopic (https://en.wikipedia.org/wiki/Ectomycorrhiza) and are particularly powerful metabolically. Whereas in other mycorrhizae the fungal cells merely infiltrate the roots, in ectomycorrhizae they form a mycelium actually replacing root tissue. Furthermore, hyphae originating at the roots reach up above the soil surface, breaking down litter such as fallen twigs by oxidising them.

It is from these 'supermycorrhizae' that most wild mushrooms and truffles (both edible and toxic) grow as reproductive structures (https://www.sciencedirect.com/science/article/abs/pii/S0065229618300880?via%3Dihub). This means that even those naturalists ignorant about microbiology have seen, and may have eaten, ectomycorrhizal fungi (https://link.springer.com/chapter/10.1007/978-3-319-53064-2_7 and https://academic.oup.com/femsre/article/31/4/388/2398987 and https://en.wikipedia.org/wiki/Truffle).

That ectomycorrhizae are effectively 'supermicorrhizae' is evident in the fact that many of the fastest-growing trees useful to humans, such as pines, oaks, poplars, eucalypts, dipterocarps and casuarinas (https://www.academia.edu/27848967/Ectomycorrhizas_in_plant_communities), depend on these associations. Most of the timber and paper we use comes from plantations nourished via ectomycorrhizal mutualisms.

Africa includes vast areas of miombo woodland (https://en.wikipedia.org/wiki/Miombo), dominated by ectomycorrhizal trees (https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/j.1469-8137.1982.tb03398.x). However, the only species penetrating South Africa are two species of Brachystegia (restricted to a few marginal locations, http://www.soutpansberg.com/brachystegia/), one species of Afzelia (sparsely distributed in the north of the country, https://en.wikipedia.org/wiki/Afzelia_quanzensis), and perhaps Manilkara.

Although most of South Africa lies at the same latitudes as lands dominated by ectomycorrhizal trees such as pines, oaks and eucalypts, it naturally lacked ecological counterparts for these trees. Ectomycorrhizae were even absent from South African species of the genera Salix and Myrica, which are ectomycorrhizal elsewhere.

The lack of ectomycorrhizae in South Africa is consistent with the odd treelessness (http://pza.sanbi.org/vegetation/fynbos-biome and http://pza.sanbi.org/vegetation/nama-karoo-biome) of this country under mediterranean-type and semi-arid climates, where the dominant plants are heath-like shrubs belonging to families (e.g. Asteraceae) and genera (e.g. Erica) unassociated with this type of mutualism.

By contrast, ectomycorrhizae are common in similar climates in Australia (https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/j.1469-8137.1980.tb00768.x), even where trees are scarce. For example, in mesic heathlands ectomycorrhizal Myrtaceae include small shrubs (e.g. see https://florabase.dpaw.wa.gov.au/browse/profile/5365). And in semi-arid scrub some of the acacias in Australia are ectomycorrhizal.

Part of the explanation may be the abundance - even by African standards - of indigenous herbivores in South Africa.

Worldwide, vegetation dominated by ectomycorrhizal plants tends to have sparse populations of herbivores, an obvious example being the boreal forest - where spruces, firs, larches, alders, willows and birches are all ectomycorrhizal.

There is likely to be a fundamental incompatibility between the nutrient-recycling regime associated with faeces and urine, and that associated with fungal decay. The former emphasises bacteria and anaerobic decomposition conserving organic matter in the soil, whereas the latter emphasises macroscopic 'white rot' and aerobic decomposition in which organic matter is wasted.

And a previously overlooked link in any explanation of the biogeographical anomaly is as follows:

South Africa is one of the few lands on Earth where fungus-culturing termites (Isoptera: Termitidae: Macrotermitinae: Odontotermes, https://www.inaturalist.org/observations/38179116 and https://www.inaturalist.org/observations/66913664) penetrate temperate climates. These insects feed litter, including coarse faeces of herbivores, to underground cultures of the fungus Termitomyces. The fungal culture produces small food-bodies eaten by the termites as well as unusually large mushrooms eaten by humans, and the rapidly recycled nutrients act as fertiliser.

Fungus-culturing termites, by removing surface litter, effectively extend the realm of herbivory at the expense of the sort of decomposition that would favour 'supermycorrhizae'. Whereas ectomycorrhizal fungi promote trees, the fungi mutualistic with macrotermitines are equally powerful in promoting a different form of recycling of nutrients, which favours grasses and herbivores.

In summary:

South Africa was - until the anthropogenic establishment of trees introduced from other continents - unsuitable for ectomycorrhizae. And part of the reason may be that it was the only land on Earth combining temperate climates with a regime of consumption of plant material in which diverse large herbivores, together with various termites operating beyond the usual roles of such insects, precluded the nutritional regime essential to ectomycorrhizae.

Posted by milewski milewski, November 04, 2021 11:29

Comments

The following intercontinental comparison deserves attention: https://www.anbg.gov.au/fungi/case-studies/desert-truffles-aust.html and https://www.jstor.org/stable/40390486.

Posted by milewski 6 months ago (Flag)

The following shows that fungus-culturing termites also occur at relatively high latitudes in China: https://en.wikipedia.org/wiki/Odontotermes_formosanus.

Posted by milewski 6 months ago (Flag)

The following is about the most northerly record for fungus-culturing termites in India: https://www.inaturalist.org/observations/21511128.

Posted by milewski 6 months ago (Flag)

Thank you for the highly interesting insight
Wolf

Posted by wolfachim 6 months ago (Flag)

Wow, you have increased my understanding today! Thank you. I have a few questions for you to consider. #1 Does Afzelia still require ectomycorrhizae? it would be interesting to find out. I know it can be grown very easily by cutting a branch and planting it making sure it has lots of water. #2. Now that most of the large herbivores are gone....? What ought we be doing to conserve? Are you aware that a number of South African trees have gone underground presumably to deal with the issue of fires. The "pyrogenic geoxylic suffrutices" https://www.gardendesign.com/plants/notables/underground-forest.html I wonder if they play into your story somehow. Thank you for reaching out, I really appreciate it. Len

Posted by lendebeer 6 months ago (Flag)

@lendebeer Hi Len, you are most welcome. Here are some detailed references to the role of fungi in seedlings of Afzelia: https://europepmc.org/article/med/33874289 and https://www.researchgate.net/publication/315311147_Ectomycorrhizal_synthesis_on_seedlings_of_Afzelia_quanzensis_Welw_using_various_types_of_inoculum and https://link.springer.com/article/10.1007/s00572-003-0276-z and https://www.jstor.org/stable/2556717. The following hints that the natural regeneration of Afzelia may be limited by the requirements of seedlings: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5870347/. I will answer your other question shortly. Best wishes from Antoni

Posted by milewski 6 months ago (Flag)

@wolfachim Hi Wolf, I'm so glad you found it worthwhile.

Posted by milewski 6 months ago (Flag)

@lendebeer Hi again Len, w.r.t. herbivores, is it not likely that the wild species have more or less been functionally replaced, in this context, by domestic livestock? W.r.t. pyrogenic geoxylic suffrutices: I plan on devoting one or more Posts to this topic in future. However, for now I've reminded myself of the genera involved (https://repository.up.ac.za/bitstream/handle/2263/49453/Maurin_Savanna_2014.pdf;jsessionid=704345BE42038A494D2C8FA0A76FFC62?sequence=1), to see how much overlap there is with the list of ectomycorrhizal genera. As it turns out, there is no overlap in the genera. The closest case is that Myrica can be ectomycorrhizal while the closely related Morella can be geoxylic. There are no caesalps in the geoxylic list, despite the presence of a few peas. Uapaca and Parinari can be ecologically comparable in tree form but the former seems always to be ectomycorrhizal whereas the latter is not, whether it grows into a tree or remains in geoxylic form. A basic ecological difference is that ectomycorrhizal plants tend to grow fast whereas geoxylic plants tend to grow slowly.

Posted by milewski 6 months ago (Flag)

Hi Antoni, I agree with you that the role of the wild herbivores has been usurped by domestic livestock, but many of the large browzers like Elephant, Black rhino, Giraffe etc have no counterpart, unless we consider goats to be partially capable in this respect. It leaves somewhat of a gaping hole in the ecology.

Posted by lendebeer 6 months ago (Flag)

Fascinating journal, thank you.

Posted by wynand_uys 6 months ago (Flag)

@wynand_uys Hi Wynand, I'm so glad that you find this kind of discussion worthwhile.

Posted by milewski 6 months ago (Flag)

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