Species interaction and recycling in ant-made fungal patches

Many tropical ant species are famous for their mutualistic relationship with plants. The host plants provide nesting space and food, the inhabiting ants in return defend the host against herbivores, pathogens and encroaching vegetation. Usually tropical ants living in a symbiosis with plants have also strong relationships with fungi cultivated in so-called fungal patches. The ants protect and nourish the fungi and occasionally feed hyphae to their larvae. In addition to fungi, the ant-associated patches are inhabited by nematodes, bacteria and archaea, presumably comprising a community with extensive cross-species interactions. Foundress ants bring fungi with them from their home nest and the fact that new queens start stockpiling parenchyma as inoculum for fungiculture straight away is testament to the fungicultures importance in the colonys survival. We suggest the fungal patches to have important functions in nutrient recycling and nutrient availability. Therefore we will investigate how the fungal patch community contributes to macronutrient recycling, nutrient provision of the ant colony, and, consequently, to the stability of the ant-plant system. Our aim is to explore whether fungal patches are nutrient-storage reservoirs which are which are refilled through the recycling of ant waste continually deposited onto the patches and to ascertain that this reservoirs are exploited by the ants for food. Explaining the function of fungi in antplant symbioses may help to understand how, despite their small size, ants are among the most successful organisms in tropical environments.

The number of interactions between species is considerable, particularly in the tropics. A remarkable interaction of different organisms is observed in the mutualistic relationships between plants and arboreal ants. The latter offer the plants protection from predators and competitors as well as nutrients from their waste. In return, the host plants provide nesting space in hollow plant structures and food. In most tropical ant-plant associations worldwide, the inhabiting ants make so-called "patches" inside the plants. At the time of colonisation, these consist of plant tissue; in larger colonies, mainly the exoskeletons of dead ants are added, but also faeces and waste. The function of these patches in the hollow plant structures remains largely unknown. However, we hypothesised that they represent crucial sites for nutrient storage and recycling in an otherwise nutrient-poor environment. To test this, we analysed the inhabitants (bacteria, fungi, nematodes) and functional processes of the patches in one of the most ubiquitous and successful ant-plant mutualisms, the Azteca-Cecropia system. For bacteria and fungi, we found in early ant colony stages low diversity and no ant species-specific community composition. However, in older colonies, the bacterial and fungal communities were highly diverse. An acquisition from the environment as well as substrate diversification may have contributed to this increase. In contrast nematode diversity is remarkably consistent. Interestingly, the bacterial, fungal and nematode communities are specific to each ant species. This means that the ant species, but not the host plant species, influence who lives in the patches. Even closely related ant species differ significantly in terms of the organisms with which they co-exist. What is the function of the patches and their organismal diversity in the ant colonies? In all ant species and at all colony developmental stages, fixation of atmospheric nitrogen by bacteria occurs, making significant amounts of nitrogen available. As the larvae feed on patch particles this can not only promote the growth of the microbial community and nematodes, but also the growth of the ant population. N2 fixation represents a previously unknown potential for arboreal ants to overcome N limitations typical of tropical rainforest canopies. Furthermore, we found evidence that the microbial communities can degrade the two most important substrates of the patches: cellulose and chitin. An analysis of the genomic information of the bacterial microbiome revealed that the ability to degrade polysaccharides is diverse and widespread. The patches can be regarded as a waste recycling system similar to the human compost heap. Finally, we showed that air-cleaning from volatiles takes place in the nest. This is important for the fragile larvae which are not protected by an exoskeleton. The project was an important step in understanding the peculiar ant-made patches.