Decline in soil quality by niche construction by two ectomycorrhizal truffle species

Niche construction requires environmental modifications by organisms, which influence selection pressures leading to evolutionary responses in a population. Niche construction has been reported for animals and plants but hardly in fungi, although mutualistic symbioses of mycorrhizal fungi could be excellent examples. So far, there are no studies on soil chemical changes caused by niche construction of ectomycorrhizal fungi, such as T. aestivum and T. melanosporum (truffles), based on long-term observations in natural forests. In the ’Alto Tajo’ Natural Park (Central Spain), 263 brûlés have been monitored for at least nine years in three oak forest types in a Mediterranean calcareous region. Brûlés are the sites where these Tuber species grow and inhibit non-host plants, soil organisms, and other mycorrhizal fungal species. The results showed that the development in the brûlé area significantly modified the soil properties and increased both Tuber species’ fitness (sporocarp production), albeit in somewhat different ways. Compared to soils outside brûlés, T. aestivum brûlés increases soil pH and decreases total carbonate and total organic carbon (TOC), whereas T. melanosporum brûlés increases active carbonate, active/total carbonate ratio, and exchangeable Ca2+, and decreases total carbonate and TOC. Therefore, the results met the two Matthews criteria that allow us to recognize niche construction by T. aestivum and T. melanosporum. However, enhanced carbonate weathering by truffles decreased soil quality because of increased soil pH, which would reduce Fe availability, and hence, host tree productivity would be limited because of an increased likelihood of chlorosis. This would indicate that mutualistic niche construction does not benefit both partners equally. Moreover, experiments adding Ca salts increased root tips and leaves of the seedlings of host plants, opening new hypotheses on eco-evolutionary mechanisms of mutualism and new approaches to rhizoculture.