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Fungal Connections Between Plants and Biocrusts Facilitate Plants But DETTWEILER-ROBINSON ET AL. Journal of Ecolog y | 895 KEYWORDS 15N translocation, Ascomycota, biological soil crusts, bunchgrass, C:N, carbon use efficiency, drylands, fungal loop hypothesis 1 | INTRODUCTION other microbially driven processes (Barger, Weber, Garcia-Pichel, Zaady, & Belnap, 2016). Similar to the microbial loop in oceans, spe- In ecosystems with low-resource availability, the retention of nutri- cies interactions that promote resource retention in drylands could ents in a living biotic pool can increase productivity. For example, slow losses, thereby increasing productivity (Bardgett & Wardle, ocean bacteria rapidly process resources from dead organisms at 2010). higher trophic levels before they sink, thereby retaining nutrients The fungal loop hypothesis proposes that networks of fungal in the photic zone (the ‘microbial loop’; Azam et al., 1983; Fenchel, hyphae link the resource dynamics of spatially and temporally dis- 2008). In tropical forests, soil fungi can translocate and retain limit- connected biocrusts and plants to promote productivity (Collins et ing nutrients in mineral-poor soils and prevent leaching during large al., 2008; Rudgers et al., 2018). Fungi are in or adjacent to both pro- rain events (Hättenschwiler, Coq, Barantal, & Handa, 2011; Lodge, ducer groups, with plant rhizospheres and biocrusts sharing 25%– 1993). In low productivity ecosystems, microbes control resources 50% of their fungal taxa (Porras-Alfaro, Herrera, Natvig, Lipinski, & in living biotic pools before releasing nutrients to primary producers; Sinsabaugh, 2011; Steven, Gallegos-Graves, Yeager, Belnap, & Kuske, in contrast, plants in mesic systems can derive nutrients from the soil 2014). Thus, the possibility exists for these shared fungi to connect solution that has been processed by microbes from the accumulated plants with biocrusts. Fungi could couple the activities of plants and soil organic matter (de Deyn, Cornelissen, & Bardgett, 2008; Knops, biocrusts temporally if they take up water or nutrients under con- Bradley, & Wedin, 2002). It is important to understand these micro- ditions when only some producers are active, such as after a light bially driven processes in low-resource ecosystems to make better rain, then transport these resources to other producers when they predictions of biogeochemical cycling and primary production. become active, such as after a large rain. Depending on the precipi- Drylands may present a unique case of microbial controls on tation regime, this fungal coupling could be more or less important to productivity because there is strong spatial and temporal heteroge- primary production. Fungi can be active at lower soil moistures than neity in resources needed for primary production. The key limiting plants (Allen, 2007; Marusenko, Huber, & Hall, 2013), supporting resource – water – is delivered in pulsed events that activate differ- their potential role as a resource reserve. Fungal hyphae may sup- ent primary producers depending on timing and amount (Collins et port more efficient translocation of resources than other potential al., 2014), potentially decoupling the activities of different producers mechanisms because movement of water and nutrients through hy- and allowing resource losses from the system. The dominant primary phae is faster than through dry soil (Frey, Six, & Elliott, 2003; Ruth, producers in drylands are vascular plants and phototrophic members Khalvati, & Schmidhalter, 2011), though diffusion and mass flow may of biological soil crusts (‘biocrusts’, diverse communities of cyano- also move resources under moist conditions. Additionally, fungi may bacteria, mosses, lichens and algae), but their activities are often act as highways that promote the movement of soil bacteria and ar- separated in both space and time. Plants occur in a patchy spatial chaea (Warmink, Nazir, Corten, & Elsas, 2011). Stable isotope tracer distribution and biocrusts occupy the soil surfaces in between plants studies have shown that N and C substrates can be translocated (interspaces). Plants generate the majority of organic matter (Aguilar between plants and biocrusts (reviewed by Rudgers et al., 2018), & Sala, 1999) and are limited secondarily by nitrogen (N; Austin et but the mechanisms of these transfers have not been documented al., 2004; Ladwig et al., 2012). Biocrusts fix atmospheric carbon (C), and could involve fungi, roots, other microbes or physical processes. and in some cases N too (Belnap, 2002). The spatial separation be- Given previous evidence that a common group of root-associated tween biocrusts on surface interspaces and plant roots deeper in soil fungi in drylands, the ‘dark septate endophytes’, generally improve means N released from biocrusts may not be accessible to plants. plant fitness (reviewed by Newsham, 2011), complex interactions Temporal separation of plant and biocrust activities may depend among plants, fungi and biocrusts may promote productivity in dry- on rainfall patterns. Only large rain events (>5 mm) sufficiently in- lands. To our knowledge, the importance of and ecological conse- crease soil moisture in the rooting zone to activate plant photosyn- quences of fungal connections for nutrient dynamics and production thesis (Huxman et al., 2004; Pockman & Small, 2010). In contrast, under different precipitation regimes have not been resolved for any biocrusts can use rain events of all sizes, although very small events dryland ecosystem. cause net losses of C because biocrusts do not remain active long We used field mesocosms in which fungal connections between enough to replace the carbon that was used to initiate photosyn- biocrusts and plant roots remained intact or were impeded for 2 years thesis (Belnap, Phillips, & Miller, 2004). N produced or immobilized to investigate three questions related to the fungal loop hypothesis. by biocrusts during times that plants are not active may be lost from (Q1) Do fungi transfer N from biocrusts to plants? N movement through the system (Belnap, 2002; Veluci, Neher, & Weicht, 2006) through or along fungal hyphae should be more rapid than through other pro- physical processes such as volatilization, photodegradation (Austin cesses, such as diffusion or independent movement by single-celled & Vivanco, 2006) and erosion (Peterjohn & Schlessinger, 1990) or microbes. (Q2) Do fungal connections improve resource reserves, and does 896 | Journal of Ecology DETTWEILER-ROBINSON ET AL. this effect vary with precipitation regime? If fungi transport N along a gra - water uptake in B. gracilis (Allen, 1982), thus fungal-mediated re- dient of availability (biocrusts with high N to plants with low N), then source transfer could also occur. C:N of plants and biocrusts should converge when fungal conn ections are present, with higher N in plants than in the absence of con nec- tions, which, in turn, will support more productivity. If C is reciprocally 2.2 | Mesocosm design transferred from plants to microbes in the biocrusts in return for N, then overall microbial carbon use efficiency should be less C limited We manipulated fungal connections (intact vs. impeded) and precipi- when intact fungal connections permit the transfer of res ources be- tation regime (small, frequent vs. large, infrequent watering events) tween biocrust and rhizosphere. If C transferred from t he rhizosphere in a full-factorial design, withn = 20 replicates per treatment combi- benefits, the photosynthetic organisms in biocrusts (pote ntially indi- nation (Figure S1). In the field, we collected biocrusts p(to 0.5–1 cm cating mixotrophy; Selosse, Charpin, & Not, 2017), the biocr usts may of soil) from around individualB. gracilis onto plastic trays then trans - be more productive and the taxa that are able to fix N (e.g. Nos tocales) planted the plants with intact rooting zone soil into plast ic pots (7.6 L) could produce more bioavailable N. Biocrust cyanobacteria may also in July–August 2013. We targeted plants that were 2–3 cm in r oot decrease their allocation to photosynthesis if plant-deri ved carbon is crown diameter (estimated shoot biomass of ~5 g) to increase t rans- available. If fungi are active during periods of low soil mois ture when plant survival compared to smaller plants. Pots were buried i nto the other organisms are not active, the benefit of fungal conn ections to ground to expose mesocosms to ambient temperature and prec ipi- resource reserves (in our study C and N) should be strongest during tation regimes. The plot was fenced to exclude large herbivo res but moist conditions when other organisms become limited by r esources was uncovered so that all pots received ambient rainfall. P ots were other than water. (Q3) Do fungal connections increase the biomass of arranged ~50 cm apart in a randomized 15 × 20 grid (an additio nal plants and/or biocrusts, and does this effect vary with precipitation regime? 200 pots in the grid were used for a related plant-biocrust i nterac- When fungal connections are intact, plant biomass and the photosyn- tion experiment; see Dettweiler-Robinson, Sinsabaugh, & Ru dgers, thetic potential of biocrusts should be higher than when connections 2018). A timeline of set-up and sampling is provided in Table S2. are impeded. If fungi ameliorate the stress of small rains to the plants and biocrusts, then fungal connections may be more important to re- source retention and productivity under precipitation regimes of many, 2.2.1 | Fungal connection treatment small rain events than regimes of few, large events.
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