In 1988, small fungal structures were found on beloved Protea flowers, endemic to South Africa. The fungal structures were identified as ophiostomatoid fungi, and besides being confined to the plants infructescence, or fruiting head, literally nothing was known about their ecology. Nearly 30 years later, with the advancement of technology and a few driven individuals focused on describing how these species function, we now finally have some answers. Who would have thought that this small, unassuming fungus would have such a complex ecology? I have learned about tripartite interactions, and thought that those were farfetched. Well, the natural world just keeps on surprising us.
Plants in the genus Protea are critically important in the functioning of shrubland ecosystems that exist in the Western Cape of South Africa. These shrublands or ‘fynbos’ ecoregions are similar to Mediterranean type ecosystems and are home to some of the most plant species rich places in all of Africa. Species of Protea are some the larger plants to grow in the area, so they are vital in plant water relations, driving supplies of water from depths many plants can’t access to the surface, in a process called hydraulic lift. Also, these plants produce large, nectar bearing flowers that support a huge array of insect and bird species, which are also vital to the pollination and dispersal of many other plants native to these systems.
Protea caffra and its white infructescence.
The decline of these plants is a result of humans altering natural fire regimes. Just until the past 20 years or so, most fires blazing in these ecosystems would be put out. The seeds of serotinous plants like in Protea species lie dormant in the seed bank until a fire rolls over them so with a compromised fire regime, these species took a major hit. Now, with a comprehensive ecological understanding of these plants, one can easily see that any possible threat to these keystone species must be identified and described. The only reason why I’m writing about this fungal endophyte now, is because grant money was dumped into many of these projects over the last 10 years, in the face of a potential threat to these ecosystems.
Most ophiostomatoid fungi are plant parasites and pathogens that are vectored by insects like beetles. The most famous ecosystem altering ophiostomatoid fungi is Ophiostoma ulmi, the culprit of Dutch elm disease. Ophiostoma ulmi spores hitch a ride from elm bark beetles that burrow beneath the trees bark and inoculate the tree. Elms evolving outside of this pathogens native Asian region have not developed any means of defense to the fungus or its vector, so eventually, they swiftly succumb to the pathogen. The fungus first discovered living on infructescences of Protea species is a sister group to the Ophiostomatales and its genus has been recently named Knoxdaviesia. Since its initial discovery, two new Ophiostoma species have been isolated from Protea flowers. With these newly described species being so closely related to the agent of Dutch elm disease, their ecology needed to be closely analyzed.
Beetle galleries. These beetles inoculated this Wych elm with Ophiostoma ulmi.
As it turns out, the ophiostomatoid fungi inhabiting these flowers are not detrimental to the plant, and may actually provide protection. By living as a saprotroph in the plants infructescences, these fungi outcompete for space against other fungi that may reduce the plants fitness. Lee et al. 2005 found that the infructescences that were not colonized by ophiostomatoid fungi had significantly higher fungal richness, and had a better chance of succumbing to fungal pathogens that could ultimately reduce seed viability. Initially, these newly described ophiostomatoid fungi were assumed to be pathogenic, but in reality, they’re plant mutualists. Now that the role of fungus was confirmed, researchers still didn’t know how the fungus was dispersed. Unlike most airborne fungal spores, the spores of these species have an adhesive pad adapted for vector dispersal. So, what is dispersing these fungi? This is when it gets interesting.
First, the scarab beetles that frequent Protea flowers for pollen and nectar where analyzed. Although a low frequency of the ophiostomatoid fungi DNA was found on three beetle species, results were not conclusive. Researchers then turned to the tiny mites that too love the conditions with Protea infructescences. Three genera of mites (Tarsonemus, Proctolaelaps and Trichouropoda) were closely analyzed for any signs of vector competence. Intact spores of ophiostomatoid fungi were isolated directly from these mites, and observed through microscopy. We found our fungal vector!
A mite from the family Tarsonemidae.
After studying these mites, researchers found that they could survive and carry out their life cycle by solely feeding on these fungi. So, in essence, these mites are a bit analogous to other insects that farm fungus. Could it be that the protection these fungi provide the plant is actually a result of mites removing unwanted organisms to protect their fungal crop? It is not an uncommon strategy among fungal farmers, but this would be the first description of mites applying these strategies.
These mites are the fungal vector we were looking for, but with their small size, there’s no way they could traverse large distances to disperse to other Protea infructescences. That’s where our scarab beetles come in. These mites carrying spores travel from flower to flower using their commensal beetle counterpart.
This is the first time I have come across a quadripartite ecology. Ophiostomatoid fungi and Protea plants are in a mutual relationship as the plant provides the fungi with a moist niche made of dead plant tissue it can feed on, while the fungi provide protection against other organisms by outcompeting for space. Ophiostomatoid fungi and three mite species are mutualists as the fungi gains a dispersal agent and possibly a manicured environment, while the mites acquire a food source. And finally, the mites and scarab beetles are in a commensal relationship, with mites gaining a dispersal agent while the beetles are largely unaffected. Four species are at play here on a single surface of a South African Flower. It makes me wonder, what else is out there?