Jake Dalzell

Ants visit a Sea Campion flower infected by a *Microbotryum* smut
fungus.

Disease is something few people love. There are exceptions though,
particularly among those who appreciate the diversity and ecological
role of plant disease. The early conservationist, Aldo Leopold,
described the role of tree diseases in creating food and shelter for the
animals on his farm in Wisconsin:

> Soon after I bought the woods a decade ago, I realized that I had
> bought almost as many tree diseases as I had trees. My woodlot is
> riddled by all the ailments wood is heir to.
>
> In October my grouse are often stuffed with oak galls... But for
> heart-rots, there would be no hollow oaks to furnish wild bees with
> oaken hives... My pileated woodpeckers chisel living pines, to extract
> fat grubs from the diseased heartwood. My barred owls find surcease
> from crows and jays in the hollow heart of an old basswood; but for
> this diseased tree their sundown serenade would probably be silenced.
>
> The real jewel of my disease-ridden woodlot is the prothonotary
> warbler. He nests in an old woodpecker hole, or other small cavity, in
> a dead snag overhanging water. The flash of his gold-and-blue plumage
> amid the dank decay of the June woods is in itself proof that dead
> trees are transmuted into living animals, and vice versa. When you
> doubt the wisdom of this arrangement, take a look at the prothonotary.
>
> Leopold, Aldo. 1949. "A Mighty Fortress." In *A Sand County Almanac &
> Other Writings on Ecology and Conservation*, edited by Curt Meiner,
> 68-71. New York: Library of America.

I met Chris Preston, a Cambridgeshire botanist, when I was in the first
year of my degree. We were at a botanical walk in one of the many
fragments of ancient woodland that dot the landscape of southern
England. He hadn't just come for botany though -- he was on the hunt for
plant pathogens. I was amazed at how he conjured them up out of thin
air, at their subtle beauty and how common they were. Since then [I have
started recording pathogens more systematically around
Belfast](https://irishplants.org/plant_pathogens.html){data-type="link"
data-id="https://irishplants.org/plant_pathogens.html"}, and have
realised that they are far more diverse than I ever realised.

<figure class="wp-block-image size-full">
<img
src="https://irishplants.org/images/plant_pathogens/april/24_04_03_Uromyces_ficariae.jpg"
class="wp-image-583" loading="lazy" decoding="async"
sizes="(max-width: 1295px) 100vw, 1295px" width="1295" height="1752" />
<figcaption>Uromyces ficariae, a common pathogen on Lesser
Celandine (Ficaria verna)</figcaption>
</figure>

At the right time of year a walk around any urban area is guaranteed to
show up at least 2 or 3 conspicuous pathogens. With some knowledge of
which plants to check you can find 20 or 30 in an afternoon (walking
around with Chris I realise just how much expert knowledge helps with
finding inconspicuous species). The diversity of these organisms in many
places begins to rival that of their hosts -- and that's just the ones
you can see.

In fact, there are far more fungi living inside plants than will ever be
visible to the naked eye. Ten or twenty leaf samples of a plant species
can yield through genetic analysis over a hundred fungal species^1^!
These fungi can be parasites (harming the plant), mutualists (benefiting
the plant), or commensals (having no effect). Some fungi can help and
hinder the plant at different stages in their life cycle.

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<img
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<img
src="https://irishplants.org/images/plant_pathogens/march/24_03_27_Golovinomyces_asperifolii3.jpg"
class="wp-image-12" loading="lazy" decoding="async" data-id="12"
sizes="(max-width: 2560px) 100vw, 2560px" width="300" height="300" />
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**1**: A conidiophore (fruiting structure) of *Peronospora ficariae*, an
oomycete pathogen of Lesser Celandine. The rounded structures are
conidia (spores). 
**2**: Conidiophores of *Golovinomyces asperifolii*, a fungal pathogen
of Forget-Me-Not (*Myosotis*). In this case the rounded cells at the end
are the conidia, and break off to disperse.

Although they may seem simple, unsophisticated organisms, many pathogens
manipulate their hosts in complex and exacting ways. Biotrophs,
pathogens which parasitise their host without killing its cells, must
avoid triggering the plant's defenses while extracting sustenance to
grow and reproduce. A few rusts even manipulate the host's development
to force it to produce *pseudoflowers*, structures which attract insects
that spread the fungus's spores^2^. That pathogens can cause plants to
produce novel structures for their own benefit is testament to their
intricate coevolution with their hosts.

<figure class="wp-block-image size-full">
<img
src="https://upload.wikimedia.org/wikipedia/commons/2/2c/Puccinia_on_Arabis.jpg"
class="wp-image-583" loading="lazy" decoding="async"
sizes="(max-width: 1295px) 100vw, 1295px" width="1295" height="1752" />
<figcaption>Puccinia monoica, an American rust which causes its
Draba host to produce pseudoflowers. Lesfreck at English
Wikipedia, <a href="https://creativecommons.org/licenses/by/3.0">CC BY
3.0</a>, via Wikimedia Commons.</figcaption>
</figure>

Besides their own diversity, diseases play a central role in the
maintenance of plant biodiversity. For a long time it was a mystery why
trees in tropical forests are so incredibly diverse, despite most of
them being ecologically very similar. In the 1970s two ecologists,
Janzen and Connell, independently explained this: species-specific
diseases can prevent any single species from becoming dominant. As the
density of a species increases, diseases specific to it spread more
rapidly, and more young plants die or never germinate. This leads to an
upper limit on how dominant any one species can be, creating gaps for
other species and meaning many more trees can coexist than would
otherwise.

The importance of disease in maintaining plant biodiversity becomes
obvious when pathogens are removed. When fungicide is sprayed in an
ecosystem, fungal diseases no longer limit the populations of plants.
Diversity and evenness decrease, with groups like grasses and sedges
benefiting from their freedom from disease and becoming more dominant.
In an alpine grassland in China it has been shown that fungi are more
important in this regard than oomycetes^3^.

Just as diseases of wild plants have existed inconspicously for most of
human history, they are also slipping away without much attention from
conservationists. Their conservation status is rarely considered, but in
Wales the smuts and allied fungi have been reasonably systematically
surveyed and assessed, with a Red List published in 2018^4^. **44% were
found to be threatened or extinct**, more than double that of any other
assessed group of plants or fungi. In fact, their incredible
specialisation on their plant hosts is their downfall, in a period of
increasing habitat loss and homogenisation. Specialists are vulnerable
to the extinction of their hosts -- when the host is lost, its pathogens
are too as a *secondary extinction*. More specialist species rely on
fewer host species and so are more vulnerable to extinction^5^. Worse,
pathogens are still vulnerable even if the host does not go extinct.
Most pathogens do not infect every host; their population fluctuates.
This means if host populations fall below some threshold the pathogen
can go extinct simply through random chance, as none of the available
host plants happen to be infected (*stochastic extinction*).

Even species on common hosts can be surprisingly rare: Lesser Celandine
(*Ficaria verna*) hosts a leaf smut, *Urocystis ficariae*, with just a
few tens of records from Britain (it is not known from Ireland but may
well be present). Other pathogens that infect this species, like
*Entyloma ficariae* and *Uromyces ficariae*, are nearly ubiquitous. It
is hard to see why something which infects such a common host should be
so rare but the problem of conserving it remains. Could even a moderate
decline in *Ficaria* put *Urocystis* at risk of stochastic extinction?
These are the consequences of declines in common species which we rarely
consider.

Beyond fascination in their endless diversity, my interest in plant
pathogens has taken me into community ecology, the study of how sets of
species assemble and change over time and space. I want to look at how
different habitats support different pathogen species, even when the
same hosts are present. In particular I think ancient and recently
created grasslands are likely to differ substantially -- it may take
many years for pathogen communities to form, and if a host is relatively
rare it may be very difficult for pathogens to disperse to newly created
habitat. Could this mean the maintenance of plant diversity by pathogens
is weaker in younger grasslands?

I hope to inspire other people to pay more attention to these maligned,
ignored organisms. I think they are really special and deserve to be
recognised as such. The clearest indication of how overlooked they are
is how easy it is to find new species to Ireland -- I have found at
least three in just a few weeks during this Easter holiday. I leave you
with a picture of *Albugo leimonios* on Cuckooflower (*Cardamine
pratensis*), which is currently my favourite pathogen-host combination.

<figure class="wp-block-image size-full">
<img
src="https://irishplants.org/images/plant_pathogens/april/24_04_12_Albugo_leimonios.jpg"
class="wp-image-583" loading="lazy" decoding="async"
sizes="(max-width: 1295px) 100vw, 1295px" width="1295" height="1752" />
<figcaption>Albugo leimonios on Cardamine pratensis in
Clement Wilson Park in the Lagan Valley. New to Ireland 12th
April 2024.</figcaption>
</figure>

## References {#references .wp-block-heading}

1. G. S. Gilbert, I. M. Parker, "Community ecology" in *The
 Evolutionary Ecology of Plant Disease*, 1st Ed., (Oxford University
 Press, 2023), pp. 203--222.
2. B. A. Roy, Floral mimicry by a plant pathogen. *Letters to Nature*
 **362** (1993).
3. X. Liu, I. M. Parker, G. S. Gilbert, Y. Lu, Y. Xiao, L. Zhang, M.
 Huang, Y. Cheng, Z. Zhang, S. Zhou, Coexistence is stabilized by
 conspecific negative density dependence via fungal pathogens more
 than oomycete pathogens. *Ecology* **103** (2022).
4. R. G. Woods, A. O. Chater, P. A. Smith, R. N. Stringer, D. A. Evans,
 *Smut and Allied Fungi of Wales: A Guide, Red Data List and Census
 Catalogue = Y Gwir-Barddu a Ffyngau Perthynol Cymru : Arweiniad,
 Rhestr Ddata Coch a Chatalog Cyfrifiad* (A.O. Chater, Aberystwyth,
 2018).
5. K. D. Lafferty, Biodiversity loss decreases parasite diversity:
 theory and patterns. *Philosophical Transactions of the Royal
 Society B: Biological Sciences* **367**, 2814--2827 (2012).

Disease is something few people love. There are exceptions though, particularly among those who appreciate the diversity and ecological role of plant disease. The early conservationist, Aldo Leopold, described the role of tree diseases in creating food and shelter for the animals on his farm in Wisconsin:  I met Chris Preston, a Cambridgeshire botanist, when I was in the first year of my degree.

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In Defence of Disease