21st Century Guidebook to Fungi, SECOND EDITION, by David Moore, Geoffrey D. Robson and Anthony P. J. Trinci

Table of Contents

1. Chapter 14: Fungi as pathogens of plants
2. Chapter 15: Fungi as symbionts and predators of animals
   1. Fungal co-operative ventures
   2. Ant agriculture
   3. Termite gardeners of Africa
   4. Agriculture in beetles
   5. Anaerobic fungi and the rise of the ruminants
   6. Nematode-trapping fungi
   7. Chapter 15 References and further reading
   8. Buy a PDF of Chapter 15
3. Chapter 16: Fungi as pathogens of animals, including man

15.1 Fungal co-operative ventures

We have already discussed the circumstance in which fungi are used as food for grazing animals, from cattle weighing hundreds of kilograms to the microarthropods weighing hundredths of a gram (see Section 11.1). Lichens (Cladonia spp.) form an essential part of the winter diet of Caribou and Reindeer (Rangifer tarandus), and the reindeer, which are ruminants, have behavioural and anatomical adaptations enabling them to graze lichens under snow cover for their resident microbiota to digest the fragments (Kumpula, 2001; Turunen et al., 2013). Fungus fruit bodies are eaten by many animals, but notably by mammals weighing less than three kilos. The dependence of animals on fungi as a food resource varies between species, but even mammals as large as deer and primates benefit by supplementing their diet with fungal fruit bodies (Hanson et al., 2003; Trierveiler-Pereira et al., 2016).

Many invertebrates use fungal mycelium as a major part of their nutrition, with approximately 80% of the tens of thousands of microarthropod species in forest soils being fungivores (or mycophagous) that depend on the fungal mycelium as their main or only food source. The many small animals involved have been mentioned in Section 11.1 (see Fig. 11.11). At the microscopic level, some of the smallest grazers on fungi are the soil organisms discussed in Section 11.2; collembola, mites, nematodes and larvae of mushroom flies. The integrated nature of mycelial networks ensures that in many fungi a morphological reaction occurs in response to grazing that serves to limit the damage caused. This implies that even at this level there is an evolutionary link between the grazing animal and the fungus. Indeed, collembola may even be perceived as mutualistic under some circumstances as they sometimes promote extra growth of the fungus as it overcompensates for grazing damage, producing a net increase in biomass, though this happens only when sufficient nutrients are available to the fungus (Bretherton et al., 2006; Ngosong et al., 2014; Põldmaa et al., 2016).

Another factor known to influence the presence of collembola in soil is the presence of endophytic fungi in the leaves of grass growing on the soil. Leaf litter infected with fungal endophytes appears to decompose faster than uninfected plant matter, possibly due to the presence of toxins changing the composition of soil communities to produce a higher proportion of detritivores (Lemons et al., 2005). Endophytes deter larger animals, such as cattle, from grazing, thereby performing a protective function for their host plants (see Chapter 13) but in so doing they are also interacting with the animals by determining the palatability, digestibility or nutritional value of their food source.

Most of the above discussion concentrates on animals using fungi as a nutritional resource, but that last paragraph raises ‘host protection’ as another function for associations between microbes and animals which has been described as defensive symbiosis. All organisms are threatened by aggressive encounters with predators, pathogens and parasites, but it is becoming increasingly evident that microbial symbionts can make important contributions to the arsenal of chemicals the host can use to defend themselves.

Many of these defensive compounds are produced by the host animals themselves, but they do take advantage of the immense chemical potential of microbial secondary metabolism and these microbial defensive symbioses are widespread. Unfortunately, most are bacterial symbionts and defensive symbiotic partnerships between animals and fungi are rarely studied. Yet they are a promising research target as fungi have a vast biosynthetic potential and are already a rich source of antibiotics (Flórez et al., 2015).

Another promising research topic that has emerged recently concerns the fungal associates of sessile marine animals; corals, sponges and tunicates. Metagenomic and transcriptomic analyses have revealed residential as well as transient and variable fungal communities. The ecological function of fungi in association with sessile marine animals is complex and there is evidence for the full range of detrimental and beneficial interactions between fungi and their marine hosts. Based on evidence from terrestrial ecosystems a rich variety of relationships is likely to be found in sessile organisms of the marine environment. The evaluation of marine animal-fungal symbioses under changing environmental conditions may prove to be critical for predicting marine ecosystem responses to global pollution and climatic change (Yarden, 2014; Amend et al., 2019 ); Chapter 16 will describe a case where the relationship has tipped over into an emerging infectious disease.

Our next topic in this Chapter, fungus farming (or gardening) by animals, is a classic mutualism, but this time with the fungus encouraging grazing rather than attempting to deter the fungivore.

Updated September, 2020