Subordinate plants mitigate drought effects on soil ecosystem processes by stimulating fungi

Abstract

Summary The subordinate insurance hypothesis suggests that highly diverse communities contain greater numbers of subordinate species than less diverse communities. It has previously been reported that subordinate species can improve grassland productivity during drought, but the underlying mechanisms remain undetermined. Using a combination of subordinate species removal and summer drought, we show that soil processes play a critical role in community resistance to drought. Interestingly, subordinate species drive soil microbial community structure and largely mitigate the effect of drought on grassland soil functioning. Our results highlight subordinate species in shifting the balance within the phospholipid fatty acid (PLFA) microbial community towards more fungal dominance. Fungal communities promoted by subordinate species were more resistant to drought and maintained higher rates of litter decomposition and soil respiration. These results emphasize the important role of subordinate species in mitigating drought effects on soil ecosystem functions. Reciprocal effects between fungi and subordinate species explain also how subordinate species better resisted to drought conditions. Our results point to a delayed plant–soil feedback following environmental perturbation. Additionally, they extend the diversity insurance hypothesis by showing that more diverse communities not only contain species well adapted to perturbations, but also species with higher impacts on soil microbial communities and related ecosystem functions.

Stoichiometric N:P flexibility and mycorrhizal symbiosis favour plant resistance against drought

“…In our drought experiment, the biomass of dominant species considerably decreased under water stress while it remained constant for the subordinate species. These results confirm findings from previous grassland experiments showing that subordinate species are more drought-resistant than dominant species (Kardol et al 2010;Mariotte et al 2013Mariotte et al , 2015. However, the underlying processes involved in the better drought resistance of subordinate species have remained unclear (Mariotte et al 2013).…”

“…The degree of AM fungal symbiosis and the dynamic of C and N in the plant-mycorrhiza system depend on the C:N balance in the plant, where the availability of one element influences the ability of plants and fungi to acquire the other (Miller et al 2002;Johnson 2010). Since dominant species control the majority of the resources, subordinate species (i.e., conservative species) generally have limited access to N and tend to accumulate C (Grigulis et al 2013;Mariotte et al 2015). Therefore, we suggest that the strong symbiotic association between AM fungi and the subordinate C. dactylon was related to the high availability of C to supply AM fungi (see Appendix S2; Kiers et al 2011) and the strong N demand of C. dactylon, as well as the high drought-tolerance of the AM fungi (see also de Vries et al 2012;Barnard, Osborne & Firestone 2013).…”

“…Among three dominant species, those with higher stoichiometric homeostasis for N responded the least to decreased soil water availability (Yu et al 2015). Conversely, in recent field experiments it was shown that dominant species are the most sensitive species to water stress while subordinate species can maintain or increase their biomass under drought (Kardol et al 2010;Mariotte et al 2013), thus promoting grassland stability (Mariotte et al 2015. These findings suggest that higher stoichiometric N:P homeostasis does not necessarily enhance plant resistance against drought, especially when contrasting dominant with subordinate species.…”

“…), thus promoting grassland stability (Mariotte et al . , ). These findings suggest that higher stoichiometric N:P homeostasis does not necessarily enhance plant resistance against drought, especially when contrasting dominant with subordinate species.…”

“…Plant carbon (C) is generally in excess when soil resources, such as N and P, limit photosynthesis, and the excess C is therefore exchanged with the arbuscular mycorrhizal (AM) fungi for N and P van der Heijden et al 2015). Interestingly, due to lower competitive abilities for nutrient uptake, subordinate species tend to accumulate more C than dominant species and have been shown to exert stronger associations with AM fungi (van der Heijden et al 1998;Urcelay & D ıaz 2003;Mariotte et al 2013Mariotte et al , 2015. Fungi are known to tolerate water stress (de Vries et al 2012;Barnard, Osborne & Firestone 2013) and root colonization by AM fungi often increases under drought (Aug e 2001), thus benefiting the survival and growth of the host plant (Worchel, Giauque & Kivlin 2013).…”