Are fungal networks key to dryland primary production?

Rudgers, Jennifer A.; Dettweiler‐Robinson, Eva; Belnap, Jayne; Green, Laura; Sinsabaugh, Robert L.; Young, Kristina E.; Cort, Catherine; Darrouzet‐Nardi, Anthony

doi:10.1002/ajb2.1184

Cited by 22 publications

(22 citation statements)

References 21 publications

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“…Diffusion should have occurred equally between the two treatments because the mesh treatment did not affect water content, and thus there may have been some role of fungal connections between biocrusts and roots that enhanced N transfer in some cases. Results support prior observations that N moves faster than can be explained by physical processes alone (Rudgers et al, ). Although there was no evidence of transfer to leaves by 30 hr, at 72 hr, there were trends that showed reduced transfer to roots when fungal connections were impeded.…”

Section: Discussionsupporting

confidence: 89%

“…The fungal loop hypothesis proposes that networks of fungal hyphae link the resource dynamics of spatially and temporally disconnected biocrusts and plants to promote productivity (Collins et al, ; Rudgers et al, ). Fungi are in or adjacent to both producer groups, with plant rhizospheres and biocrusts sharing 25%–50% of their fungal taxa (Porras‐Alfaro, Herrera, Natvig, Lipinski, & Sinsabaugh, ; Steven, Gallegos‐Graves, Yeager, Belnap, & Kuske, ).…”

Section: Introductionmentioning

confidence: 99%

“…Additionally, fungi may act as highways that promote the movement of soil bacteria and archaea (Warmink, Nazir, Corten, & Elsas, ). Stable isotope tracer studies have shown that N and C substrates can be translocated between plants and biocrusts (reviewed by Rudgers et al, ), but the mechanisms of these transfers have not been documented and could involve fungi, roots, other microbes or physical processes. Given previous evidence that a common group of root‐associated fungi in drylands, the ‘dark septate endophytes’, generally improve plant fitness (reviewed by Newsham, ), complex interactions among plants, fungi and biocrusts may promote productivity in drylands.…”

Section: Introductionmentioning

confidence: 99%

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Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts

2019

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1. Species interactions may couple the resource dynamics of different primary producers and may enhance productivity by reducing loss from the system. In low-resource systems, this biotic control may be especially important for maintaining productivity. In drylands, the activities of vascular plants and biological soil crusts can be decoupled in space because biocrusts grow on the soil surface but plant roots are underground, and decoupled in time due to biocrusts activating with smaller precipitation events than plants. Soil fungi are hypothesized to functionally couple the plants and biocrusts by transporting nutrients. We studied whether disrupting fungi between biocrusts and plants reduces nitrogen transfer and retention and decreases primary production as predicted by the fungal loop hypothesis. Additionally, we compared varying precipitation regimes that can drive different timing and depth of biological activities.2. We used field mesocosms in which the potential for fungal connections between biocrusts and roots remained intact or were impeded by mesh. We imposed a precipitation regime of small, frequent or large, infrequent rain events. We used 15 N to track fungal-mediated nitrogen (N) transfer. We quantified microbial carbon use efficiency and plant and biocrust production and N content. Fungal connections with biocrusts benefitted plant biomass and nutrient retentionunder favourable (large, infrequent) precipitation regimes but not under stressful (small, frequent) regimes, demonstrating context dependency in the fungal loop.Translocation of a 15 N tracer from biocrusts to roots was marginally lower when fungal connections were impeded than intact. Under large, infrequent rains, when fungal connections were intact, the C:N of leaves converged towards the C:N of biocrusts, suggesting higher N retention in the plant, and plant above-ground biomass was greater relative to the fungal connections-impeded treatment. Carbon use efficiency in both biocrust and rooting zone soil was less C-limited when connections were intact than impeded, again only in the large, infrequent precipitation regime. Synthesis.Although we did not find evidence of a reciprocal transfer of C and N between plants and biocrusts, plant production was benefited by fungal connections with biocrusts under favourable conditions. | 895 Journal of Ecology DETTWEILER-ROBINSON ET aL. | 901 Journal of Ecology DETTWEILER-ROBINSON ET aL. | 907 Journal of Ecology DETTWEILER-ROBINSON ET aL. and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Applied and Environmental Microbiology, 70(2), 973-983. https ://doi.Additional supporting information may be found online in the Supporting Information section. How to cite this article: Dettweiler-Robinson E, Sinsabaugh RL, Rudgers JA. Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts. J Ecol. 2020;108:894-907. https ://doi.

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Section: Discussionsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts

2019

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“…First, fungal symbionts can change the outcome of plant competition (Bever et al., 1997; Chung & Rudgers, 2016; Crawford et al., 2019), and so they may shape plant community dynamics. Second, fungi may be more important than bacteria for carbon and nutrient cycling in dryland ecosystems (Rudgers et al., 2018) and can be more resistant than bacteria to drought (de Vries et al., 2018; Ochoa‐Hueso et al., 2018; Wang et al., 2017). Thus, understanding fungal responses to drought may be especially critical for predicting future communities under climate change.…”

Section: Introductionmentioning

confidence: 99%

Experimental drought re‐ordered assemblages of root‐associated fungi across North American grasslands

et al. 2020

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Plant‐associated fungi can ameliorate abiotic stress in their hosts, and changes in these fungal communities can alter plant productivity, species interactions, community structure and ecosystem processes. We investigated the response of root‐associated fungi to experimental drought (66% reduction in growing season precipitation) across six North American grassland ecosystem types to determine how extreme drought alters root‐associated fungi, and understand what abiotic factors influence root fungal community composition across grassland ecosystems. Next generation sequencing of the fungal ITS2 region demonstrated that drought primarily re‐ordered fungal species' relative abundances within host plant species, with different fungal responses depending on host identity. Grass species that declined more under drought trended toward less community re‐ordering of root fungi than species less sensitive to drought. Host identity and grassland ecosystem type defined the magnitude of drought effects on community composition, diversity and root colonization, and the most important factor affecting fungal composition was plant species identity. Fungal diversity was less responsive to drought than fungal composition. Across ecosystems, latitude and soil pH were better predictors of fungal diversity than experimental drought. Drought significantly reduced fungal diversity and evenness only in sideoats grama Bouteloua curtipendula and reduced root colonization only in blue grama B. gracilis. Our results illustrate that predicting the effects of drought on root‐associated fungi will require attention to host plant identity and ecosystem type. By comparing our findings against soil microbe responses in the same experiment, we propose the hypothesis that fungi in plant roots are less sensitive to drought than fungi inhabiting soils. Our study highlights the importance of studying community‐level re‐ordering of fungal composition for understanding plant responses to climate change.

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“…In dryland systems (e.g. deserts, semi deserts, savannas, and shrublands), similar mycelial networks, termed fungal loops, may enable nutrient exchange between the two dominant producer communities: biological soil crusts (biocrusts) and vascular plants (Green et al., 2008; Rudgers et al., 2018).…”

Section: Introductionmentioning

confidence: 99%

Evidence for a fungal loop in shrublands

Janke

Coe

2021

Journal of Ecology

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Dryland communities may mitigate the loss of limited resources by exchanging nutrients through subterranean fungal connections, termed fungal loops. In arid grasslands, fungal loops can influence community composition and primary productivity, yet their ecological significance across dryland systems remains unexplored. We investigated the functional role of fungal loops in nutrient translocation in a North American shrubland ecosystem. We traced the movement of 15N from moss‐dominated biocrusts to the dominant xeric shrub Larrea tridentata, and the movement of 13C from L. tridentata to biocrusts in plots established in situ in the Sonoran Desert. Measurements occurred at three time points spanning 1 week following a simulated 2.5 mm rainfall event, and at distances up to 1 m from tracer application. We also used ITS sequencing to investigate changes in fungal community composition in soils over the 1‐week period. We discovered movement of 15N from biocrusts into L. tridentata foliage as well as 15N movement to other spatially isolated moss‐dominated biocrust patches, yet this movement did not occur until 4–6 days post‐rainfall, when significantly higher δ15N was observed in L. tridentata and biocrusts compared to previous days. We did not observe consistent patterns of 13C movement from L. tridentata into neighbouring shrubs or biocrusts, suggesting differential environmental drivers for carbon movement in this system. Fungal communities exhibited a decrease in alpha diversity on the last day of the study, indicative of a delayed community response to rainfall concomitant with nutrient translocation. Fungal endophyte orders Pleosporales and Pezizales dominated all plot soils, and order Pleosporales was significantly more abundant in 15N enriched plots, suggesting that dark septate endophytic fungi were involved in nitrogen translocation. The delay in nutrient translocation may reflect a rainfall‐triggered rebuilding of mycelial networks between community members following drought. Synthesis. Our results point to fungal‐mediated nutrient exchange pathways in a previously uninvestigated vegetation type, shrublands, where nutrients are translocated between moss‐dominated biocrusts and nearby shrubs. We provide the first evidence that nutrient transfer may be delayed up to 6 days following rainfall, consistent with pulse‐dynamic responses in drylands, and that moss‐dominated biocrusts play a role in fungal loops.

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Are fungal networks key to dryland primary production?

Cited by 22 publications

References 21 publications

Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts

Fungal connections between plants and biocrusts facilitate plants but have little effect on biocrusts

Experimental drought re‐ordered assemblages of root‐associated fungi across North American grasslands

Evidence for a fungal loop in shrublands

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