Thus, from the war of nature, from famine and death, the most exalted object which we are capable of conceiving … directly follows.
—Darwin, Charles. 1861. “Conclusion.” In On the Origin of Species, 425. New York: D. Appleton and Company.
This is true in more ways than Darwin knew. He was talking about evolution (of the “higher animals”), but not only is death a hammer by which natural selection beats species into “endless forms”, death from disease is the reason so many of these endless forms can coëxist. The outcome of increased mortality from disease is reduced competition between plant species. It is not an obvious outcome of one organism harming another, but it emerges when we consider the spatial dynamics of a population.
First, let's consider an adult tree in fruit. The seeds of the tree land all around, in decreasing amounts as we get further from the trunk. The highest density is right by the base of the tree. Seeds aren't the only thing the tree produces though. Both through the air and under the ground, spores of fungi and oömycetes are also spreading. Adult gall midges and seed weevils fly out from its canopy. Larval mites are blown on the breeze. These, too, land all around the tree, at highest density nearest the trunk, right among most of the seeds! The seeds are less likely to survive the closer they are to their parent tree. The denser the stand of trees of this species gets, the fewer survive to adulthood.
Now look at the figure below. The black line shows the density of seeds as we get further from the tree (moving right). The yellow line shows the density of species-specific pathogens. In this case, the seeds can spread further than the pathogens. As pathogens are more abundant closer to the tree, the death rate of seedlings (purple) is higher. This leads to a dip in seedling density (green) immediately around the tree.
This large dip in seedling density appears in the rather extreme case where seeds can spread further than pathogens, but it is illustrative of a more general effect. We can directly observe this in tropical tree seedlings, which have a higher death rate at higher densities unless fungal pathogens are excluded with fungicide1. The death rate immediately around the tree is higher, leading to overdispersion: adult trees are further apart from each other than we would expect based on the distribution of seeds. This is the Janzen-Connell Effect, originally described to explain the mysterious diversity of tropical trees2, most of which more-or-less do the same thing. Ecologists were confused why one species did not simply outcompete all of the others, since they all occupy a similar niche.
The Janzen-Connell Effect is one strand of a wider phenomenon known as Negative Conspecific Density Dependence (NCDD). This literally means the phenomenon where the competitive fitness of a species decreases as the density of that species increases. The Janzen-Connell Effect refers to the result of increased disease as the density of a species increases, but the same phenomenon also arises from resource competition. Two individuals of the same species use more similar resources (soil nutrients, space) than two individuals of different species. Plants are therefore usually in stronger competition with their own species than they are with other species. As the density of a species increases, an individual of that species is in stronger competition on average with the individual plants around it, as more of them are its conspecific competitors. Therefore, its competitive fitness is lower, as the resources it uses are more depleted. From a population dynamics perspective this and the Janzen-Connell effect look identical, and for that reason the Janzen-Connell effect is often thought of as effective competition between individuals of the same species. Although it is disease spread that causes it, the result is the same as actual competition.
The Janzen-Connell Effect can explain why such a high number of species can coëxist in communities like tropical forests and grasslands, despite sharing similar ecological niches, but it does not explain why so many species do exist in these communities and not others. For example, boreal forests have very low tree species diversity, with large areas of Earth being covered by just a few conifer species. This does not mean that density-dependent phenomena like the Janzen-Connell Effect are not at play here. It is simply one small part of the story, and we need to look to other parts of ecological and evolutionary theory to explain the development of diversity in these areas. That is beyond the scope of this website, but if you are interested you can find discussion of differences in biodiversity across the globe by searching for papers on the latitudinal diversity gradient, the phenomenon where biodiversity is higher at lower latitudes (the tropics). A good early discussion paper is Gaston (2000)3. More generally, the field that investigates these large-scale patterns in ecology and biodiversity is macroecology.
You may have noticed that the Janzen-Connell Effect only makes sense if the pathogens dispersing from a parent tree are more likely infect individuals of the same species (the parents' seedlings) than they are other species. It is a result of species-specific pathogens. We will see later that generalist pathogens, which infect many different species, also have a role to play in the structure of plant communities.
The Janzen-Connell Effect is part of a wider body of work known as Coëxistence Theory. This seeks to explain why, and under what circumstances, different species can coëxist. In many ways it is a field in its infancy: ecosystems are incredibly complex, and being able to predict their dynamics is not something we can do yet. What coëxistence theory has provided is a set of smaller explanations and predictions, and many of these are quite profound. Considering the Janzen-Connell effect, we see the importance of pathogens in maintaining the diversity of an ecosystem. This leads us to the prediction that in their absence, plant diversity would decrease. This is an easily testable hypothesis — we simply take a plant community, remove the pathogens, and see what happens. This is generally done using biocides, particularly fungicides. The result is exactly as we expected: when pathogens are removed, the diversity of the community decreases3. In the same experiment, it was shown that fungi are more important than oömycetes in this effect — when oömyceticide is sprayed, the decrease in diversity is less than when fungicide is sprayed.
The other major way pathogens can promote coëxistence is by reducing the competitive difference between species4. Unlike the Janzen-Connell effect, this involves generalist pathogens. Probably the best studied example of this is the parasitic plant Yellow Rattle Rhinanthus spp. It is a bit strange to think of a parasitic plant as a pathogen, but the ecology is similar to that of fungal and oömycetous pathogens: it steals resources for its own reproduction, and has a more rapid lifecycle than its hosts (being an annual plant with generally perennial hosts). It does this by forming specialised root structures called haustoria which latch on to the roots of other plants, forming a connection with the host xylem. It keeps all of its stomata open, letting lots of water out through its leaves. This creates a pressure gradient, so sap is sucked out of the roots of its host. Through the haustorium it can steal water and nutrients in the xylem sap.
By stealing resources, Yellow Rattle weakens its host. Not all hosts are equally affected though, and the resulting change in community composition has led to its reputation as the ‘meadow maker’. An increasing abundance of Yellow Rattle leads to lower productivity in grasslands5,6. It most negatively affects spreading clonal species such as grasses and other graminoids, benefiting less competitive low-growing species like forbs7. Most studies have found Yellow Rattle has positive or neutral effects on plant species richness8. The details of this illustrate more general processes that mean pathogens can promote coëxistence between plant species.
Graminoids are grasses and their close relatives sedges (Cyperaceae) and rushes (Juncaceae). The relevance of these plants to grassland ecology is that they have tall, narrow leaf blades that dominate the vertical space of a grassland, and that they generally grow rapidly, spreading by underground rhizomes to cover large areas. They are strong competitors for light in particular, and are dominant in many grassland ecosystems globally.
Forbs are herbaceous plants that are not graminoids. Most herbaceous plants have much wider leaves and are slower growing than graminoids. They are less strong competitors for light as they generally cannot dominate the vertical space of a grassland like graminoids can.
An idealised version of the shift from a plant community dominated by grasses to one dominated by forbs (herbaceous perennials) can be visualised using a dynamic spatial model9,10. This is a computer simulation, programmed with simple equations modelling how different plants compete with each other and disperse across the landscape. In this simulation, Yellow Rattle is not initially present, and the community is dominated by grasses (green). Yellow Rattle (red) is introduced and rapidly proliferates, but it reduces the grass population. As grasses are a better host for Yellow Rattle, this means it quickly runs out of effective hosts. Its population decreases and forbs (blue) become the dominant plants in the community, supporting a lower population of Yellow Rattle. The results of this model can also be visualised as a graph of proportional abundance across the ‘meadow’ shown below:
Yellow Rattle is not particularly picky about its hosts. It can parasitise most grasses and forbs (herbaceous perennials) in the grasslands where it is found, though some species can avoid being parasitised by forming strong lignin barriers in their roots, or killing tissue around the area it tries to parasitise. Why then does it reduce the competitive dominance of grasses, and not simply weaken all of the plants in the community equally? One possibility is that of physiological tradeoffs.
Physiological tradeoffs are a fundamental part of plant ecology. The idea is that rather than there being a single optimal strategy or niche a plant can occupy, different traits may exist in a tradeoff with one another, such that improvements in one are to the detriment of another. A classic example of this (and the one most relevant to pathogens mediating coëxistence) is the Growth-Resistance Tradeoff, which is where the growth rate of a plant and its ability to resist environmental pressures like disease, herbivory, and drought are negatively correlated. In a grassland, grasses employ a growth strategy, using any resources they acquire to expand rapidly. If they are eaten by herbivores, they can simply grow more leaves. In contrast, forbs tend to be slower growing, saving their resources and investing in expensive ways to deter herbivores, like toxins, hairs, and spines.