Plant pathogens are ubiquitous in terrestrial ecosystems, but their role in these ecosystems is understudied. One aspect of their ecology that has not been studied is their influence on nutrient cycling. Plant pathogens likely increase the rate of nutrient cycling in two ways: by stealing nutrients from their host plant and making them available to invertebrates in a more easily consumed form, and by reducing leaf lifespan, increasing the rate of litter entering the soil. I will now explore both of these mechanisms, the evidence for each, and potential future research directions.

Plant tissue is rich in carbon, nitrates, phosphates, and other nutrients, but these are not easily available to herbivores. Plant cell walls are formed of cellulose, a difficult to digest polymer. On top of this plants defend themselves through physical (spines, hairs, slippery bark etc) and chemical means (toxins). It is difficult for a herbivorous invertebrate to make its living by eating plants, and for this reason many are highly specialised, feeding on just one or a few species to whose defenses they have adapted.

However, when a pathogen such as a rust fungus infects a plant, it is able to sequester many of these nutrients in its own tissues, using complex biochemical mechanisms. These pathogens are often highly specialised to specific hosts themselves, and are able to manipulate their host in an exacting way to obtain nutrition without killing host tissue. They use the nutrients they steal from their host to grow and produce spores.

These spores are generally dispersed by wind or splashing water, and so must be deposited on the surface of the leaf. In general, they are poorly defended, and are thus an easily accessible food resource for invertebrates. For this reason, a large guild of invertebrates have evolved to feed on plant pathogens. Let’s refer to them as pathophagous (“disease-eating”). These are a subset of the wider set of fungivorous/mycophagous (“fungus-eating”) invertebrate species.

One iconic pathophagous insect is the 22-spot Ladybird (Psyllobora vigintiduopunctata). Like other species of mildew-feeding ladybirds, this small beetle feeds on powdery mildews, fungi in the family Erysiphaceae. The powdery mildews represent a particularly easily accessed source of stolen plant nutrients as much of their tissue is produced on the outside of the host. They form a mat of white mycelium which ladybirds and other inverterbrates graze on. All life stages of the 22-spot ladybird feed on this, and given how common they are in grasslands the volume of nutrient flows in the mildew → ladybird → predators/parasitoids system must be considerable.

Another highly specialised group of pathophagous insects is the rust-eating midges (Mycodiplosis). These tiny flies lay eggs on rust-infected leaves, and their larvae feed exclusively on rust spores. There is some species diversity within the genus but the taxonomy remains understudied, and the evidence for different species specialising on different rusts is low (Henk et al., 2011; Nelsen, 2013). How abundant are they? I don’t have much data yet, but in my fieldwork at one site I found three Mycodiplosis larvae, in two of my five 2×2m quadrats. They are certainly very common and something I regularly find while looking at microfungi.

Not all pathophagous invertebrates exclusively eat plant pathogens, and many are not widely recognised as pathophagous at all. For example, there is some evidence that some slugs preferentially feed on rust-infected leaves (Ramsell & Paul, 1990). Among the best studied system is the larvae of the moth Lymantria dispar on poplars. They preferentially feed on leaves infected by Melampsora rusts, and actually graze on the rust spores before feeding on the leaf itself. Rust spores are rich in mannitol, a sugar alcohol that can be an energy source for the larvae. They contain higher concentrations of amino acids and other nitrogen sources than host leaves. Alongside this they contain lower concentrations of defence compounds, making them easy pickings for the moth larvae (Eberl et al., 2020).

Beyond these specific examples a cursory look at a plant infected with a rust, powdery, or downy mildew makes it clear that they are an important food source for invertebrates. I regularly am frustrated in my efforts to identify pathogens that have been grazed by slugs or snails, and very often find springtails of many kinds. A lot more research is needed to understand how large of a nutrient flow this represents at the ecosystem scale, and how it differs from an ecosystem lacking pathogens.

The other important effect of pathogens on nutrient cycling is that of reduced leaf lifespan. This is little better studied than the action of pathophagous invertebrates. Oak leaves heavily infected by powdery mildew are shed considerably more quickly than healthy leaves (Hajji et al., 2009). Anecdotally I have seen that Spilopodia nervisequia, an endophyte of Plantago lanceolata, causes the leaves of its host to yellow and die in the winter, while uninfected plants remain green. Most trivially, necrotrophic pathogens by definition actively kill leaf tissue. The result is that pathogens cause leaves to enter the soil as litter earlier than they otherwise would. This effectively speeds up nutrient cycling.

How can we estimate the effect of plant pathogens on nutrient cycling? One method could be to compare communities where they are present to those where they have been excluded using fungicide and oömyceticide (Liu et al., 2022). For nitrogen, the rate of nutrient cycling can be estimated with a mechanistic model parameterised with measurements of the stable isotope ratio in plant tissues and the soil. Furthermore, the ubiquity of pathophagous invertebrates is not yet appreciated and further research on their abundance and diversity in natural ecosystems would do much to improve our understanding of their ecological importance.

This is the first essay of a series I plan on writing during my PhD, in order to consolidate my thoughts and communicate what I am studying and thinking about. I’ll tag them as PhD essays.

References

Eberl, F., Fernandez de Bobadilla, M., Reichelt, M., Hammerbacher, A., Gershenzon, J., & Unsicker, S. B. (2020). Herbivory meets fungivory: Insect herbivores feed on plant pathogenic fungi for their own benefit. Ecology Letters, 23(7), 1073–1084. https://doi.org/10.1111/ele.13506

Hajji, M., Dreyer, E., & Marçais, B. (2009). Impact of Erysiphe alphitoides on transpiration and photosynthesis in Quercus robur leaves. European Journal of Plant Pathology, 125(1), 63–72. https://doi.org/10.1007/s10658-009-9458-7

Henk, D. A., Farr, D. F., & Aime, M. C. (2011). Mycodiplosis (Diptera) infestation of rust fungi is frequent, wide spread and possibly host specific. Fungal Ecology, 4(4), 284–289. https://doi.org/10.1016/j.funeco.2011.03.006

Liu, X., Parker, I. M., Gilbert, G. S., Lu, Y., Xiao, Y., Zhang, L., Huang, M., Cheng, Y., Zhang, Z., & Zhou, S. (2022). Coexistence is stabilized by conspecific negative density dependence via fungal pathogens more than oomycete pathogens. Ecology, 103(12). https://doi.org/10.1002/ecy.3841

Nelsen, D. J. (2013). A Phylogenetic Analysis of Species Diversity, Specificity, and Distribution of Mycodiplosis on Rust Fungi [Master of Science, Louisiana State University and Agricultural and Mechanical College]. https://doi.org/10.31390/gradschool_theses.2700

Ramsell, J., & Paul, N. D. (1990). Preferential Grazing by Molluscs of Plants Infected by Rust Fungi. Oikos, 58(2), 145–150. https://doi.org/10.2307/3545421