Hyphae move matter and microbes to mineral microsites: Integrating the hyphosphere into conceptual models of soil organic matter stabilization.

Associations between soil minerals and microbially derived organic matter (often referred to as mineral-associated organic matter or MAOM) form a large pool of slowly cycling carbon (C). The rhizosphere, soil immediately adjacent to roots, is thought to control the spatial extent of MAOM formation because it is the dominant entry point of new C inputs to soil. However, emphasis on the rhizosphere implicitly assumes that microbial redistribution of C into bulk (non-rhizosphere) soils is minimal. We question this assumption, arguing that because of extensive fungal exploration and rapid hyphal turnover, fungal redistribution of soil C from the rhizosphere to bulk soil minerals is common, and encourages MAOM formation. First, we summarize published estimates of fungal hyphal length density and turnover rates and demonstrate that fungal C inputs are high throughout the rhizosphere-bulk soil continuum. Second, because colonization of hyphal surfaces is a common dispersal mechanism for soil bacteria, we argue that hyphal exploration allows for the non-random colonization of mineral surfaces by hyphae-associated taxa. Third, these bacterial communities and their fungal hosts determine the chemical form of organic matter deposited on colonized mineral surfaces. Collectively, our analysis demonstrates that omission of the hyphosphere from conceptual models of soil C flow overlooks key mechanisms for MAOM formation in bulk soils. Moving forward, there is a clear need for spatially explicit, quantitative research characterizing the environmental drivers of hyphal exploration and hyphosphere community composition across systems, as these are important controls over the rate and organic chemistry of C deposited on minerals.

Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition.

Interactions between symbiotic ectomycorrhizal (EM) and free-living saprotrophs can result in significant deceleration of leaf litter decomposition. While this phenomenon is widely cited, its generality remains unclear, as both the direction and magnitude of EM fungal effects on leaf litter decomposition have been shown to vary among studies. Here we explicitly examine how contrasting leaf litter types and EM fungal communities may lead to differential effects on carbon (C) and nitrogen (N) cycling. Specifically, we measured the response of soil nutrient cycling, litter decay rates, litter chemistry and fungal community structure to the reduction of EM fungi (via trenching) with a reciprocal litter transplant experiment in adjacent Pinus- or Quercus-dominated sites. We found clear evidence of EM fungal suppression of C and N cycling in the Pinus-dominated site, but no suppression in the Quercus-dominated site. Additionally, in the Pinus-dominated site, only the Pinus litter decay rates were decelerated by EM fungi and were associated with decoupling of litter C and N cycling. Our results support the hypothesis that EM fungi can decelerate C cycling via N competition, but strongly suggest that the 'Gadgil effect' is dependent on both substrate quality and EM fungal community composition. We argue that understanding tree host traits as well as EM fungal functional diversity is critical to a more mechanistic understanding of how EM fungi mediate forest soil biogeochemical cycling.

Global patterns in fine root decomposition: climate, chemistry, mycorrhizal association and woodiness.

Fine root decomposition constitutes a critical yet poorly understood flux of carbon and nutrients in terrestrial ecosystems. Here, we present the first large-scale synthesis of species trait effects on the early stages of fine root decomposition at both global and local scales. Based on decomposition rates for 279 plant species across 105 studies and 176 sites, we found that mycorrhizal association and woodiness are the best categorical traits for predicting rates of fine root decomposition. Consistent positive effects of nitrogen and phosphorus concentrations and negative effects of lignin concentration emerged on decomposition rates within sites. Similar relationships were present across sites, along with positive effects of temperature and moisture. Calcium was not consistently related to decomposition rate at either scale. While the chemical drivers of fine root decomposition parallel those of leaf decomposition, our results indicate that the best plant functional groups for predicting fine root decomposition differ from those predicting leaf decomposition.

Estimating uncertainty in the volume and carbon storage of downed coarse woody debris.

Downed coarse woody debris, also known as coarse woody detritus or downed dead wood, is challenging to estimate for many reasons, including irregular shapes, multiple stages of decay, and the difficulty of identifying species. In addition, some properties are commonly not measured, such as wood density and carbon concentration. As a result, there have been few previous evaluations of uncertainty in estimates of downed coarse woody debris, which are necessary for analysis and interpretation of the data. To address this shortcoming, we quantified uncertainties in estimates of downed coarse woody debris volume and carbon storage using data collected from permanent forest inventory plots in the northeastern United States by the Forest Inventory and Analysis program of the USDA Forest Service. Quality assurance data collected from blind remeasurement audits were used to quantify error in diameter measurements, hollowness of logs, species identification, and decay class determination. Uncertainty estimates for density, collapse ratio, and carbon concentration were taken from the literature. Estimates of individual sources of uncertainty were combined using Monte Carlo methods. Volume estimates were more reliable than carbon storage, with an average 95% confidence interval of 15.9 m3 /ha across the 79 plots evaluated, which was less than the mean of 31.2 m3 /ha. Estimates of carbon storage (and mass) were more uncertain, due to poorly constrained estimates of the density of wood. For carbon storage, the average 95% confidence interval was 11.1 Mg C/ha, which was larger than the mean of 4.6 Mg C/ha. Accounting for the collapse of dead wood as it decomposes would improve estimates of both volume and carbon storage. On the other hand, our analyses suggest that consideration of the hollowness of downed coarse woody debris pieces could be eliminated in this region, with little effect. This study demonstrates how uncertainty analysis can be used to quantify confidence in estimates and to help identify where best to allocate resources to improve monitoring designs.

Soil nitrogen affects phosphorus recycling: foliar resorption and plant-soil feedbacks in a northern hardwood forest.

Previous studies have attempted to link foliar resorption of nitrogen and phosphorus to their. respective availabilities in soil, with mixed results. Based on resource optimization theory, we hypothesized that the foliar resorption of one element could be driven by the availability of another element. We tested various measures of soil N and P as predictors of N and P resorption in six tree species in 18 plots across six stands at the Bartlett Experimental Forest, New Hampshire, USA. Phosphorus resorption efficiency (P < 0.01) and proficiency (P = 0.01) increased with soil N content. to 30 cm depth, suggesting that trees conserve P based on the availability of soil N. Phosphorus resorption also increased with soil P content, which is difficult to explain basdd on single-element limitation, butfollows from the correlation between soil N and soil P. The expected single-element relationships were evident only in the 0 horizon: P resorption was high where resin-available P was low in the Oe (P < 0.01 for efficiency, P < 0.001 for proficiency) and N resorption was high where potential N mineralization in the Oa was low (P < 0.01 for efficiency and 0.11 for proficiency). Since leaf litter is a principal source of N and P to the 0 horizon, low nutrient availability there could be a result rather than a cause of high resorption. The striking effect of soil N content on foliar P resorption is the first evidence of multiple-element control on nutrient resorption to be reported from an unmanipulated ecosystem.

Melanization slows the rapid movement of fungal necromass carbon and nitrogen into both bacterial and fungal decomposer communities and soils.

Microbial necromass contributes significantly to both soil carbon (C) persistence and ecosystem nitrogen (N) availability, but quantitative estimates of C and N movement from necromass into soils and decomposer communities are lacking. Additionally, while melanin is known to slow fungal necromass decomposition, how it influences microbial C and N acquisition as well as elemental release into soils remains unclear. Here, we tracked decomposition of isotopically labeled low and high melanin fungal necromass and measured 13C and 15N accumulation in surrounding soils and microbial communities over 77 d in a temperate forest in Minnesota, USA. Mass loss was significantly higher from low melanin necromass, corresponding with greater 13C and 15N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in 13C and/or 15N at all sampling points, with enrichment being consistently higher on low melanin necromass and earlier in decomposition. Similar patterns of preferential C and N enrichment of many bacterial and fungal genera early in decomposition suggest that both microbial groups co-contribute to the rapid assimilation of resource-rich soil organic matter inputs. While overall richness of taxa enriched in C was higher than in N for both bacteria and fungi, there was a significant positive relationship between C and N in co-enriched taxa. Collectively, our results demonstrate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate but also necromass C and N release and that both elements are rapidly co-utilized by diverse bacterial and fungal decomposers in natural settings. IMPORTANCE Recent studies indicate that microbial dead cells, particularly those of fungi, play an important role in long-term carbon persistence in soils. Despite this growing recognition, how the resources within dead fungal cells (also known as fungal necromass) move into decomposer communities and soils are poorly quantified, particularly in studies based in natural environments. In this study, we found that the contribution of fungal necromass to soil carbon and nitrogen availability was slowed by the amount of melanin present in fungal cell walls. Further, despite the overall rapid acquisition of carbon and nitrogen from necromass by a diverse range of both bacteria and fungi, melanization also slowed microbial uptake of both elements. Collectively, our results indicate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate, but also necromass carbon and nitrogen release into soil as well as microbial resource acquisition.

Quantifying uncertainty in annual runoff due to missing data.

Long-term streamflow datasets inevitably include gaps, which must be filled to allow estimates of runoff and ultimately catchment water budgets. Uncertainty introduced by filling gaps in discharge records is rarely, if ever, reported. We characterized the uncertainty due to streamflow gaps in a reference watershed at the Hubbard Brook Experimental Forest (HBEF) from 1996 to 2009 by simulating artificial gaps of varying duration and flow rate, with the objective of quantifying their contribution to uncertainty in annual streamflow. Gaps were filled using an ensemble of regressions relating discharge from nearby streams, and the predicted flow was compared to the actual flow. Differences between the predicted and actual runoff increased with both gap length and flow rate, averaging 2.8% of the runoff during the gap. At the HBEF, the sum of gaps averaged 22 days per year, with the lowest and highest annual uncertainties due to gaps ranging from 1.5 mm (95% confidence interval surrounding mean runoff) to 21.1 mm. As a percentage of annual runoff, uncertainty due to gap filling ranged from 0.2-2.1%, depending on the year. Uncertainty in annual runoff due to gaps was small at the HBEF, where infilling models are based on multiple similar catchments in close proximity to the catchment of interest. The method demonstrated here can be used to quantify uncertainty due to gaps in any long-term streamflow data set, regardless of the gap-filling model applied.