This is a book to justify why pathogens are worthy of study, outside of their role as crop pests. It is about their diversity, beauty, and importance. It is quite skeletal at the minute, so watch this space as it grows!
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.
When you hear the word disease, what do you think? Fear and disgust are common reactions to a term that conjures images of death and human suffering. In natural ecosystems, however, disease is just another ecosystem function that emerges when one organisms attacks another. A pathogen infecting a plant is functionally very similar to a caterpillar eating its leaves, and is there really that much difference between “insect destroyer” fungi killing flies and birds eating them?
The visceral response to disease comes from our own experiences with human pathogens. When we see an animal predator eating insects or a herbivore grazing we can often relate to this process, but who can identify with a fungus? It is only when we start to look for these organisms in garden, grasslands, and woodlands that we realise how diverse and ubiquitous they are. In an afternoon walk it is often easy to find fifteen or twenty different pathogens infecting many of the commonest plants in the landscape. Most of these pathogens do not kill their host, but alter its development in complex and sometimes beautiful ways for their own benefit.
A single plant species like Devil's-bit Scabious Succisa pratensis can have many different pathogens. On a single visit to Murlough National Nature Reserve, I found three different species infecting its flowers, representing three distant branches of the tree of life: Fungi, Oömycota, and Insecta. The first, Microbotryum succisae, is a smut fungus. It alters the development of the anthers, replacing the pollen they would normally produce with its own bright white spores. It is easy to spot while wandering through a field of Scabious, the pale halo of an infected flowerhead standing ghostly against the purple background. This is just one of many smut fungi that infect the flowers, fruits, and leaves of a host of different flowering plants. Like most flower smuts, it is spread by pollinators: more on that later.
The second species I encountered at Murlough was more subtle at first. I noticed a flowerhead that had large, warm purple flowers. This really caught my eye as it contrasted in colour and size with the surrounding plants. Taking a closer look, I was surprised to find the tiny conidiophores of a downy mildew in the genus Peronospora growing on the petals. These oömycetes are a common pathogen on the leaves of many grassland plants, but finding them on flowers is rarer. A small subset of species, known as the floricolous downy mildews, have evolved to grow at very low densities throughout the tissue of their hosts, only emerging to produce spores on the petals of the flowers. This species, P. violacea, has taken this further by completely changing the morphology of the flowers: the anthers abort early in development and do not produce any pollen, and the ovary is shrunken and does not produce seeds1. The petals are nearly double the size of those on an uninfected plant, and are distinctly redder. I suspect the colour change is caused by a change in pH, as anthocyanin pigments that colour most flowers change colour depending on the pH. All of these changes further the oömycete's goal: to attract pollinators that will spread its sticky spores to uninfected plants.
While wandering around the reserve, entranced by these wonderful pathogens, I noticed many plants had flowers that seemed late to open, and did not open in the normal order. The flowers at the top and bottom of a head of Devil's-bit Scabious are the first to open, with a band around the middle last. In some plants this day, I noticed that a few flowers were still closed even as those in the same band or further towards the middle were already open. Eventually I had seen enough to know it was not just a random abberation, so I stopped to investigate. Carefully opening up these unopened flowers revealed small orange larvae. Looking on the Plant Parasites of Europe page for the host, I found Contarinia dipsacearum was a match. Until this record it had been seen just once in Britain and Ireland, in 1947 in London2. The adult fly lays its eggs in the developing flower buds, and the larvae gall the flowers, preventing the buds from opening. This provides a safe, humid home for them as they develop. Eventually, they leave their flower to pupate in the soil, before emerging as adults to restart the whole process.
Three very different organisms have converged on the flowers of one plant to survive and reproduce. Even beyond this, a look at the rest of the plant reveals still further diversity. A small kink in the stem is caused by the thin white net of Erysiphe knautiae, a powdery mildew fungus. The leaves are covered in purple dots: leaf spot fungi in the genus Septoria. Around the Scabious, countless other pathogens are growing, reproducing, and dying on every plant species you can see. Rusts burn orange welts on leaves and stems. Leaf spot fungi sneak through stomata into their hosts' leaves. Tiny chytrid zoöspores swim through films of water to reach new territory on leaves and roots.
This overwhelming diversity is vital to the normal function of terrestrial ecosystems. Plant pathogens keep the populations of their hosts in check, promoting coëxistence and increasing plant diversity. By causing host tissue to die earlier than it otherwise would, they change the dynamics of nutrient cycling. Both powdery and downy mildews are eaten by springtails and ladybirds that are specialised to feed on them.
These interactions are changing. Climate change is causing warmer, drier conditions across much of the world. Eutrophication is shifting the competitive dynamics between plant species. Human introductions are bringing plants and their pathogens across the world. In Wales, the only place where the conservation status of whole groups of pathogens has been assessed, many are threatened with local extinction3,4, and this is likely the case in much of the rest of the world. Other pathogens are jumping to new hosts, sometimes causing functional or actual extinction.
I hope I have piqued your interest in these fascinating, misunderstood organisms. The topics I have touched on here I will go into in more detail in the coming chapters. First: a look at some of the most specialised pathogens, those spread by pollinators.