Favorable effect of mycorrhizae on biomass production efficiency exceeds their carbon cost in a fertilization experiment

Abstract

Biomass production efficiency (BPE), the ratio of biomass production to photosynthesis, varies greatly among ecosystems and typically increases with increasing nutrient availability. Reduced carbon partitioning to mycorrhizal fungi (i.e., per unit photosynthesis) is the hypothesized underlying mechanism, as mycorrhizal abundance and plant dependence on these symbionts typically decrease with increasing nutrient availability. In a mesocosm experiment with Zea mays, we investigated the effect of nitrogen (N) and phosphorus (P) addition and of mycorrhizal inoculation on BPE. Photosynthesis and respiration were measured at mesocosm scale and at leaf scale. The growth of arbuscular mycorrhizal fungi (AMF) was assessed with ingrowth bags while also making use of the difference in δ C between C plants and C soil. Mesocosms without AMF, that is, with pasteurized soil, were used to further explore the role of AMF. Plant growth, photosynthesis, and BPE were positively affected by P, but not by N addition. AMF biomass also was slightly higher under P addition, but carbon partitioning to AMF was significantly lower than without P addition. Interestingly, in the absence of AMF, plants that did not receive P died prematurely. Our study confirmed the hypothesis that BPE increases with increasing nutrient availability, and that carbon partitioning to AMF plays a key role in this nutrient effect. The comparison of inoculated vs. pasteurized mesocosms further suggested a lower carbon cost of nutrient uptake via AMF than via other mechanisms under nutrient rich conditions.

Experimental evidence that phosphorus fertilization and arbuscular mycorrhizal symbiosis can reduce the carbon cost of phosphorus uptake

“…In summer 2016, the year before the present experiment, the same mesocosms had been used in an N × P experiment. This previous experiment showed that the growth of maize in these soils was strongly limited by P availability, while N was ample as N addition did not affect plant growth (Verlinden et al, ). Nonetheless, to ensure that plant growth was not limited by N supply, 95.5 kg N/ha (calcium nitrate; YaraLiva ® Calcinit ® , Yara B.V., Rotterdam‐Vlaardingen, The Netherlands) was added to each mesocosm on 20 July 2017.…”

“…The experiment was set up in a greenhouse in Sint‐Katelijne‐Waver (Belgium, 51°04′38″N, 4°32′05″E) and consisted of 30 mesocosms with insulated walls (1 m × 1.2 m × 0.6 m high), filled with nutrient‐poor experimental soil containing C 3 plant‐derived organic matter (same soil as in Verlinden et al, ). The homogenized mixture contained (a) sandy soil (Arenosol) originating from a pine forest in a nature reserve in Belgium with a texture of 95% sand and 5% silt, mixed with (b) white river sand and (c) a minor fraction of potting soil in a proportion of 72, 23 and 5 volume %, respectively.…”

“…The probes were inserted into the soil during one week (starting on 13 July 2017) before being analysed, providing an estimate of the relative availabilities of different nutrients (e.g. Dijkstra et al, ; May et al, ; Verlinden et al, ; Vicca et al, ).…”

“…While the inverse relationship between root:shoot ratio and nutrient availability is well established (Anderson, ; Bonifas, Walters, Cassman, & Lindquist, ; Hammond & White, ; Verlinden et al, ; Vicca et al, ), other aspects of the C investment in nutrient acquisition (e.g. root exudates or mycorrhizal symbiosis) are still poorly quantified.…”

“…Compared to plant roots, mycorrhizal fungi have access to a larger portion of soil nutrients because of their large surface‐to‐volume ratio, and because they produce specific enzymes to release nutrients that are strongly bound to organic matter and minerals (Marschener, ; Sanders & Tinker, ). As a result, mycorrhizal fungi can not only consume a considerable fraction of the assimilated C (Hobbie, ; Verlinden et al, ; Vicca et al, ), but can also alter other below‐ground carbon fluxes (i.e. root respiration, turnover and exudation; Jones et al, ; King et al, ; Raven, Lambers, Smith, & Westoby, ).…”