Mechanistically-grounded pathways connect remotely sensed canopy structure to soil respiration.

Variation in the soil-to-atmosphere C flux, or soil respiration (Rs), is influenced by a suite of biotic and abiotic factors, including soil temperature, soil moisture, and root biomass. However, whether light detection and ranging (lidar)-derived canopy structure is tied to soil respiration through its simultaneous influence over these drivers is not known. We assessed relationships between measures of above- and belowground vegetation density and complexity, and evaluated whether Rs is linked to remotely sensed canopy structure through pathways mediated by established biotic and abiotic mechanisms. Our results revealed that, at the stand-scale, canopy rugosity-a measure of complexity-and vegetation area index were coupled to soil respiration through their effects on light interception, soil microclimate, and fine root mass density, but this connection was stronger for complexity. Canopy and root complexity were not spatially coupled at the stand-scale, with canopy but not root complexity increasing through stand development. Our findings suggest that remotely sensed canopy complexity could be used to infer spatial variation in Rs, and that this relationship is grounded in known mechanistic pathways. The broad spatial inference of soil respiration via remotely sensed canopy complexity requires multi-site observations of canopy structure and Rs, which is possible given burgeoning open data from ecological networks and satellite remote sensing platforms.

Disturbance-accelerated succession increases the production of a temperate forest.

Many secondary deciduous forests of eastern North America are approaching a transition in which mature early-successional trees are declining, resulting in an uncertain future for this century-long carbon (C) sink. We initiated the Forest Accelerated Succession Experiment (FASET) at the University of Michigan Biological Station to examine the patterns and mechanisms underlying forest C cycling following the stem girdling-induced mortality of >6,700 early-successional Populus spp. (aspen) and Betula papyrifera (paper birch). Meteorological flux tower-based C cycling observations from the 33-ha treatment forest have been paired with those from a nearby unmanipulated forest since 2008. Following over a decade of observations, we revisit our core hypothesis: that net ecosystem production (NEP) would increase following the transition to mid-late-successional species dominance due to increased canopy structural complexity. Supporting our hypothesis, NEP was stable, briefly declined, and then increased relative to the control in the decade following disturbance; however, increasing NEP was not associated with rising structural complexity but rather with a rapid 1-yr recovery of total leaf area index as mid-late-successional Acer, Quercus, and Pinus assumed canopy dominance. The transition to mid-late-successional species dominance improved carbon-use efficiency (CUE = NEP/gross primary production) as ecosystem respiration declined. Similar soil respiration rates in control and treatment forests, along with species differences in leaf physiology and the rising relative growth rates of mid-late-successional species in the treatment forest, suggest changes in aboveground plant respiration and growth were primarily responsible for increases in NEP. We conclude that deciduous forests transitioning from early to middle succession are capable of sustained or increased NEP, even when experiencing extensive tree mortality. This adds to mounting evidence that aging deciduous forests in the region will function as C sinks for decades to come.

Exploring the role of ectomycorrhizal fungi in soil carbon dynamics.

The extent to which ectomycorrhizal (ECM) fungi enable plants to access organic nitrogen (N) bound in soil organic matter (SOM) and transfer this growth-limiting nutrient to their plant host, has important implications for our understanding of plant-fungal interactions, and the cycling and storage of carbon (C) and N in terrestrial ecosystems. Empirical evidence currently supports a range of perspectives, suggesting that ECM vary in their ability to provide their host with N bound in SOM, and that this capacity can both positively and negatively influence soil C storage. To help resolve the multiplicity of observations, we gathered a group of researchers to explore the role of ECM fungi in soil C dynamics, and propose new directions that hold promise to resolve competing hypotheses and contrasting observations. In this Viewpoint, we summarize these deliberations and identify areas of inquiry that hold promise for increasing our understanding of these fundamental and widespread plant symbionts and their role in ecosystem-level biogeochemistry.

Decadal post-fire succession of soil invertebrate communities is dependent on the soil surface properties in a northern temperate forest.

Although fires are common disturbances in North American forests, the extent to which soil invertebrate assemblages recover from burning remains unclear. Here, we examine long-term (14- to 101-yr) recoveries of soil invertebrate communities from common cut and burn treatments conducted at 6 to 26-yr intervals since 1911 in a deciduous forest in the upper Great Lakes region (USA). We characterize soil surface macro-invertebrate communities during both fall and spring across a long-term, experimental fire chronosequence to characterize invertebrate community recovery at decadal time-scales and community changes between seasons. We posited that changes in invertebrate community structure might, in turn, impact decomposition process. We sampled active organisms at the soil surface using pitfall traps. We described understory vegetation, measured soil properties, and conducted a 4-year litter bag study with big-toothed aspen leaves (Populus grandidentata). Invertebrate community responses followed a habitat accommodation model of succession showing that invertebrate succession is dependent on the soil surface properties. The fall and spring measures revealed that the densities of active invertebrates were highest 101 years after fire. For a given pair of stands, a pattern of sharing higher percentage of taxa was denoted when stands were of similar age. Some species such as the beetle Stelidota octomaculata appeared to be indicator of the chronosequence succession stage because it tracks the successional increase of Quercus and acorn production at the study site. We also found a significant positive correlation between leaf decomposition of soil macrofaunal accessible leaves and millipedes density across the chronosequence. We show that vegetation cover changes and related shifts in habitat structure occurring during post-fire succession are important in shaping communities assemblages. This finding highlights the importance of simultaneously considering abiotic-biotic factors together with above- and belowground measurements to better characterize controls on successional community dynamics after disturbance.

Effects of canopy structure and species diversity on primary production in upper Great Lakes forests.

Canopy structure and tree species diversity, shaped by succession, disturbance, and community composition, are linked to numerous ecosystem functions, including net primary production (NPP). Understanding of how ecosystem structural metrics are interrelated and mechanistically link to NPP, however, is incomplete. We characterized leaf area index (LAI), Simpson's index of Diversity (D', a measure of species diversity), and canopy rugosity (Rc, a measure of canopy physical complexity) in 11 forest stands comprising two chronosequences varying in establishing disturbance, and in three late successional communities. We related LAI, D', and Rc to wood NPP (NPPw), and examined whether absorption of photosynthetically active radiation and light use-efficiency (LUE) link NPPw with ecosystem structure. We found that recovery of LAI and D' was delayed following more severe establishing disturbances, but that the development of Rc was strikingly conserved regardless of disturbance, converging on a common mean value in late-successional stands irrespective of differences in leaf area index and species diversity. LAI was significantly correlated with NPPw in each stage of ecosystem development, but NPPw was only correlated with Rc in early successional stages and with D' in late successional stages. Across all stands, NPPw was coupled with LAI and Rc, (but not D') through positive relationships with light absorption and LUE. We conclude by advocating for better integration of ecological disciplines investigating structure-function interactions, suggesting that improved understanding of such relationships will require ecologists to traverse disciplinary boundaries.

The detrital input and removal treatment (DIRT) network: Insights into soil carbon stabilization.

Ecological research networks functioning across climatic and edaphic gradients are critical for improving predictive understanding of biogeochemical cycles at local through global scales. One international network, the Detrital Input and Removal Treatment (DIRT) Project, was established to assess how rates and sources of plant litter inputs influence accumulations or losses of organic matter in forest soils. DIRT employs chronic additions and exclusions of aboveground litter inputs and exclusion of root ingrowth to permanent plots at eight forested and two shrub/grass sites to investigate how soil organic matter (SOM) dynamics are influenced by plant detrital inputs across ecosystem and soil types. Across the DIRT network described here, SOM pools responded only slightly, or not at all, to chronic doubling of aboveground litter inputs. Explanations for the slow or even negative response of SOM to litter additions include increased decomposition of new inputs and priming of old SOM. Evidence of priming includes increased soil respiration in litter addition plots, decreased dissolved organic carbon (DOC) output from increased microbial activity, and biochemical markers in soil indicating enhanced SOM degradation. SOM pools decreased in response to chronic exclusion of aboveground litter, which had a greater effect on soil C than did excluding roots, providing evidence that root-derived C is not more critical than aboveground litter C to soil C sequestration. Partitioning of belowground contributions to total soil respiration were predictable based on site-level soil C and N as estimates of site fertility; contributions to soil respiration from root respiration were negatively related to soil fertility and inversely, contributions from decomposing aboveground litter in soil were positively related to site fertility. The commonality of approaches and manipulations across the DIRT network has provided greater insights into soil C cycling than could have been revealed at a single site.

Nitrate is an important nitrogen source for Arctic tundra plants.

Plant nitrogen (N) use is a key component of the N cycle in terrestrial ecosystems. The supply of N to plants affects community species composition and ecosystem processes such as photosynthesis and carbon (C) accumulation. However, the availabilities and relative importance of different N forms to plants are not well understood. While nitrate (NO3-) is a major N form used by plants worldwide, it is discounted as a N source for Arctic tundra plants because of extremely low NO3- concentrations in Arctic tundra soils, undetectable soil nitrification, and plant-tissue NO3- that is typically below detection limits. Here we reexamine NO3- use by tundra plants using a sensitive denitrifier method to analyze plant-tissue NO3- Soil-derived NO3- was detected in tundra plant tissues, and tundra plants took up soil NO3- at comparable rates to plants from relatively NO3--rich ecosystems in other biomes. Nitrate assimilation determined by 15N enrichments of leaf NO3- relative to soil NO3- accounted for 4 to 52% (as estimated by a Bayesian isotope-mixing model) of species-specific total leaf N of Alaskan tundra plants. Our finding that in situ soil NO3- availability for tundra plants is high has important implications for Arctic ecosystems, not only in determining species compositions, but also in determining the loss of N from soils via leaching and denitrification. Plant N uptake and soil N losses can strongly influence C uptake and accumulation in tundra soils. Accordingly, this evidence of NO3- availability in tundra soils is crucial for predicting C storage in tundra.

Isotopic study of mercury sources and transfer between a freshwater lake and adjacent forest food web.

Studies of monomethylmercury (MMHg) sources and biogeochemical pathways have been extensive in aquatic ecosystems, but limited in forest ecosystems. Increasing evidence suggests that there is significant mercury (Hg) exchange between aquatic and forest ecosystems. We use Hg stable isotope ratios (δ(202)Hg and Δ(199)Hg) to investigate the relative importance of MMHg sources and assess Hg transfer pathways between Douglas Lake and adjacent forests located at the University of Michigan Biological Station, USA. We characterize Hg isotopic compositions of basal resources and use linear regression of % MMHg versus δ(202)Hg and Δ(199)Hg to estimate Hg isotope values for inorganic mercury (IHg) and MMHg in the aquatic and adjacent forest food webs. In the aquatic ecosystem, we found that lake sediment represents a mixture of IHg pools deposited via watershed runoff and precipitation. The δ(202)Hg and Δ(199)Hg values estimated for IHg are consistent with other studies that measured forest floor in temperate forests. The Δ(199)Hg value estimated for MMHg in the aquatic food web indicates that MMHg is subjected to ~20% photochemical degradation prior to bioaccumulation. In the forest ecosystem, we found a significant negative relationship between total Hg and δ(202)Hg and Δ(199)Hg of soil collected at multiple distances from the lakeshore and lake sediment. This suggests that IHg input from watershed runoff provides an important Hg transfer pathway between the forest and aquatic ecosystems. We measured Δ(199)Hg values for high trophic level insects and compared these insects at multiple distances perpendicular to the lake shoreline. The Δ(199)Hg values correspond to the % canopy cover suggesting that forest MMHg is subjected to varying extents of photochemical degradation and the extent may be controlled by sunlight. Our study demonstrates that the use of Hg isotopes adds important new insight into the relative importance of MMHg sources and complex Hg transfer pathways across ecosystem boundaries.

Sustained carbon uptake and storage following moderate disturbance in a Great Lakes forest.

Carbon (C) uptake rates in many forests are sustained, or decline only briefly, following disturbances that partially defoliate the canopy. The mechanisms supporting such functional resistance to moderate forest disturbance are largely unknown. We used a large-scale experiment, in which > 6700 Populus (aspen) and Betula (birch) trees were stem-girdled within a 39-ha area, to identify mechanisms sustaining C uptake through partial canopy defoliation. The Forest Accelerated Succession Experiment in northern Michigan, USA, employs a suite of C-cycling measurements within paired treatment and control meteorological flux tower footprints. We found that enhancement of canopy light-use efficiency and maintenance of light absorption maintained net ecosystem production (NEP) and aboveground wood net primary production (NPP) when leaf-area index (LAI) of the treatment forest temporarily declined by nearly half its maximum value. In the year following peak defoliation, redistribution of nitrogen (N) in the treatment forest from senescent early successional aspen and birch to non-girdled later successional species facilitated the recovery of total LAI to pre-disturbance levels. Sustained canopy physiological competency following disturbance coincided with a downward shift in maximum canopy height, indicating that compensatory photosynthetic C uptake by undisturbed, later successional subdominant and subcanopy vegetation supported C-uptake resistance to disturbance. These findings have implications for ecosystem management and modeling, demonstrating that forests may tolerate considerable leaf-area losses without diminishing rates of C uptake. We conclude that the resistance of C uptake to moderate disturbance depends not only on replacement of lost leaf area, but also on rapid compensatory photosynthetic C uptake during defoliation by emerging later successional species.

Community-specific impacts of exotic earthworm invasions on soil carbon dynamics in a sandy temperate forest.

Exotic earthworm introductions can alter above- and belowground properties of temperate forests, but the net impacts on forest soil carbon (C) dynamics are poorly understood. We used a mesocosm experiment to examine the impacts of earthworm species belonging to three different ecological groups (Lumbricus terrestris [anecic], Aporrectodea trapezoides [endogeic], and Eisenia fetida [epigeic]) on C distributions and storage in reconstructed soil profiles from a sandy temperate forest soil by measuring CO2 and dissolved organic carbon (DOC) losses, litter C incorporation into soil, and soil C storage with monospecific and species combinations as treatments. Soil CO2 loss was 30% greater from the Endogeic x Epigeic treatment than from controls (no earthworms) over the first 45 days; CO2 losses from monospecific treatments did not differ from controls. DOC losses were three orders of magnitude lower than CO2 losses, and were similar across earthworm community treatments. Communities with the anecic species accelerated litter C mass loss by 31-39% with differential mass loss of litter types (Acer rubrum > Populus grandidentata > Fagus grandifolia > Quercus rubra > or = Pinus strobus) indicative of leaf litter preference. Burrow system volume, continuity, and size distribution differed across earthworm treatments but did not affect cumulative CO2 or DOC losses. However, burrow system structure controlled vertical C redistribution by mediating the contributions of leaf litter to A-horizon C and N pools, as indicated by strong correlations between (1) subsurface vertical burrows made by anecic species, and accelerated leaf litter mass losses (with the exception of P. strobus); and (2) dense burrow networks in the A-horizon and the C and N properties of these pools. Final soil C storage was slightly lower in earthworm treatments, indicating that increased leaf litter C inputs into soil were more than offset by losses as CO2 and DOC across earthworm community treatments.

Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska.

Long-term fertilization of acidic tussock tundra has led to changes in plant species composition, increases in aboveground production and biomass and substantial losses of soil organic carbon (SOC). Root litter is an important input to SOC pools, although little is known about fine root demography in tussock tundra. In this study, we examined the response of fine root production and live standing fine root biomass to short- and long-term fertilization, as changes in fine root demography may contribute to observed declines in SOC. Live standing fine root biomass increased with long-term fertilization, while fine root production declined, reflecting replacement of the annual fine root system of Eriophorum vaginatum, with the long-lived fine roots of Betula nana. Fine root production increased in fertilized plots during an unusually warm growing season, but remained unchanged in control plots, consistent with observations that B. nana shows a positive response to climate warming. Calculations based on a few simple assumptions suggest changes in fine root demography with long-term fertilization and species replacement could account for between 20 and 39% of the observed declines in SOC stocks.

Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra.

Ecologists have long been intrigued by the ways co-occurring species divide limiting resources. Such resource partitioning, or niche differentiation, may promote species diversity by reducing competition. Although resource partitioning is an important determinant of species diversity and composition in animal communities, its importance in structuring plant communities has been difficult to resolve. This is due mainly to difficulties in studying how plants compete for below-ground resources. Here we provide evidence from a 15N-tracer field experiment showing that plant species in a nitrogen-limited, arctic tundra community were differentiated in timing, depth and chemical form of nitrogen uptake, and that species dominance was strongly correlated with uptake of the most available soil nitrogen forms. That is, the most productive species used the most abundant nitrogen forms, and less productive species used less abundant forms. To our knowledge, this is the first documentation that the composition of a plant community is related to partitioning of differentially available forms of a single limiting resource.

A 15N tracer technique for assessing fine root production and mortality.

We tested a 15N tracer technique to assess fine root production and mortality based on temporal measurements of the 15N mass in fine root structural tissues and the 15N concentration of the plant-available soil N pool. The results of a pilot study indicated that this technique is based on sound methods and reasonable assumptions. The 15N tracer technique avoids most of the major limitations which hinder existing methods and may provide valuable insight into the rates and controls of fine root production and mortality in terrestrial ecosystems.

Immobilization of a 15N-labeled nitrate addition by decomposing forest litter.

Effects of chronic HNO3 and H2SO4 additions on decomposition of senesced birch leaf, beech leaf, spruce needle, and wood chip litters were examined. Litters were incubated for up to 4 years in fiberglass mesh (1 mm) bags on experimental plots in a mixed-species forest near the Bear Brooks Watershed Manipulation (BBWM) site in eastern Maine, United States. Plot treatments included HNO3 additions at 28 and 56 kg N·ha-1·year-1, H2SO4 additions at 128 kg S·ha-1·year-1, and a combined HNO3 and H2SO4 treatment at 28 kg N and 64 kg S ·ha-1·year-1. The 15N content of all NO3 added was artificially increased to 344% δ15N. Litter bags were collected each fall and analyzed for organic matter loss, nitrogen concentration, and 15N abundance throughout the 4-year experiment. Extractive (non-polar-soluble+water-soluble), cellulose (acid-soluble), and lignin (acid-insoluble) fractions were analyzed for the first 2 years. In wood chips, nitrogen additions increased mass loss and N concentration, but not the mass of N after 4 years. Neither N nor S additions had large effects on mass loss, N concentration, or N content of leaf litters. All litters immobilized and mineralized N simultaneously, but we were able to place a lower bound on gross N immobilization by mass balancing 15N additions. Birch and spruce litters showed net mineralization, while beech leaf and wood chip litters showed net immobilization. Net immobilizing litters were those with the highest initial cellulose concentration (wood chips=80% beech leaves=54%), and we attribute the higher capacity for immobilization to more readily available carbon. Lignin mass increased initially in all litter types except spruce needles. Also, extractives in net immobilizing litters either increased initially (wood chips) or decreased at a slower rate than bulk litter (beech leaves). We calculate the potential of decomposing litter to immobilize exogenous nitrate in this system to be 1-1.5 kg N·ha-1·year-1, which is about half of the usual NO3 deposition at this site, but only a small fraction of the experimental addition.

The fate of 15N-labelled nitrate additions to a northern hardwood forest in eastern Maine, USA.

We followed the movements of 15N-labelled nitrate additions into biomass and soil pools of experimental plots (15×15 m each) in a mid-successional beech-maple-birch-spruce forest in order to identify sinks for nitrate inputs to a forest ecosystem. Replicate plots (n=3) were spray-irrigated with either 28 or 56 kg N ha-1 year-1 using 15N-labelled nitric acid solutions (δ15N = 344‰ ) during four successive growing seasons (April-October). The 15N contents of foliage, bolewood, forests floor and mineral soil (0-5 cm) increased during the course of treatments. Mass balance calculations showed that one-fourth to one-third of the nitrate applied to forest plots was assimilated into and retained by above ground plant tissues and surface soil horizons at both rates of nitrate application. Plant and microbial assimilation were of approximately equal importance in retaining nitrate additions to this forest. Nitrate use among tree species varied, however, with red spruce showing lower rates of nitrate assimilation into foliage and bolewood than American beech and other deciduous species.

Factors Controlling Nitrogen Cycling and Nitrogen Saturation in Northern Temperate Forest Ecosystems.

An analysis of the factors controlling rates of nitrogen cycling in northern temperate forest ecosystems is presented based on a quantitative analysis of an extensive data set for forests in Wisconsin and Massachusetts as those data are synthesized in a computer model (VEGIE) of organic matter and nutrient dynamics. The model is of the "lumped-parameter," nutrient-flux-density type, dealing with major components of forest ecosystems rather than stems or species. It deals explicitly with the interactions among light, water, and nutrient availability in determining transient and equilibrium rates of primary production and nutrient cycling. Data are presented for parameterizing the plant component of the system at either the species or community level. A major conclusion is that the ultimate control on equilibrium nitrogen-cycling rates resides not within the nitrogen cycle itself (for example in litter quality or net primary production [NPP] allocation patterns) but rather in ratios of resource-use efficiency by vegetation as compared with the ratios of resource availability. Litter quality and allocation patterns, along with rates of N deposition, do affect the rate at which a system approaches the equilibrium cycling rate. The model is used to explain observed variation in nitrogen-cycling rates among forest types, and to predict the timing and occurrence of "nitrogen saturation" (N availability in excess of biotic demand) as a function of nitrogen deposition rates and harvesting.

A general biogeochemical model describing the responses of the C and N cycles in terrestrial ecosystems to changes in CO(2), climate, and N deposition.

A model that simulates carbon (C) and nitrogen (N) cycles in terrestrial ecosystems is developed. The model is based on the principle that the responses of terrestrial ecosystems to changes in CO(2), climate, and N deposition will encompass enzymatic responses, shifts in tissue stoichiometry, changes in biomass allocation among plant tissues, altered rates of soil organic matter turnover and N mineralization, and ultimately a redistribution of C and N between vegetation and soils. The model is a highly aggregated, process-based, biogeochemical model designed to examine changes in the fluxes and allocation of C and N among foliage, fine roots, stems, and soils in response to changes in atmospheric CO(2) concentration, temperature, soil water, irradiance, and inorganic nitrogen inputs. We use the model to explore how changes in CO(2) concentration, temperature, and N inputs affect carbon storage in two ecosystems: arctic tundra and temperate hardwood forest. The qualitative responses of the two ecosystems were similar. Quantitative differences are attributed to the initial distribution of C and N between vegetation and soils, to the amounts of woody tissue in the two ecosystems, and to their relative degree of N limitation. We conclude with a critical analysis of the model's strengths and weaknesses, and discuss possible future directions.

Fine root turnover in forest ecosystems in relation to quantity and form of nitrogen availability: a comparison of two methods.

Two methods of estimating fine root production and turnover are compared for 13 forest ecosystems exhibiting a wide range in form (NH4+ vs. NO3-) and quantity of available nitrogen. The two methods are by comparison of seasonal maxima and minima in biomess and by nitrogen budgeting. Both methods give similar results for stands with low rates of nitrification. The budgeting method predicts higher fine root turnover and productivity than the max-min method for systems with significant rates of nitrification.