Substrate Age Gradient Research Articles

The expanding role of deep roots during long‐term terrestrial ecosystem development

AbstractModels of ecosystem development and response to environmental variation must incorporate change in vertical soil space as well as over time. Insufficient measurement of subsurface soil properties represents a major observational bias in ecosystem studies.We address these changes in horizontal (time) and vertical (soil profile) space along a three‐million‐year, semi‐arid, piñon‐juniper woodland substrate age gradient with characteristic progressive and retrogressive ecosystem development phases and a shift from nitrogen (N) and water to phosphorus (P) limitation. We present a novel pedological approach using isotopic tracers and biogeochemical analyses to address fine root distribution, depth of plant uptake and relative nutrient availabilities.We show that (a) the quantity of fine roots remains constant with ecosystem development but their distribution in the soil profile becomes increasingly deeper and less concentrated in the surface soil; (b) mean depth of tree uptake becomes deeper with substrate age and follows the relative availability of P as P‐limitation develops and (c) soil P transformations in the oldest soil profiles resemble the theoretical changes with age to produce a depth gradient of relative N and P availability.Synthesis. The expanding role of deep roots in this model system is tightly linked to phases of ecosystem development and relative nutrient availability. The inclusion of whole soil profiles is vital to investigating the intersections of biota, soil and geologic substrate and developing a more complete understanding of ecosystem structure and function.

The increase of soil organic carbon as proposed by the “4/1000 initiative” is strongly limited by the status of soil development - A case study along a substrate age gradient in Central Europe

During COP 21 in Paris 2015, several states and organizations agreed on the “4/1000” initiative for food security and climate. This initiative aims to increase world's soil organic carbon (SOC) stocks by 4‰ annually. The influence of soil development status on SOC dynamics is very important but usually not considered in studies. We analyse SOC accumulation under forest, grassland and cropping systems along a soil age gradient (10–17,000years) to show the influence of soil development status on SOC increase.SOC stocks (0–40cm) and accumulation rates along a chronosequence in alluvial soils of the Danube River in the Marchfeld (eastern Austria) were analysed. The analysed Fluvisols and Chernozems have been used as forest, grassland and cropland for decades or hundreds of years.The results showed that there is a fast build-up of OC stocks (0–40cm) in young soils with accumulation of ~1.3tha−1a−1 OC in the first 100years and ~0.5tha−1a−1 OC between 100 and 350years almost independent of land use. Chernozems with a sediment deposition age older than 5.000years have an accumulation rate<0.01tOCha−1a−1 (0–40cm).Radiocarbon dating showed that the topsoil (0–10cm) consists mainly of “>modern” and “modern” carbon indicating a fast carbon cycling. Carbon in subsoil is less exposed to decomposition and OC can be stored at long-time scales in the subsoil (14C age of 3670±35 BP).In view of the ‘4/1000’ initiative, soils with constant carbon input (forest & grassland) fulfil the intended 4‰ growth rate of SOC stocks only in the first 60years of soil development. We proclaim that under the present climate in Central Europe, the increase of SOC stocks in soil is strongly affected by the state of soil development.

No evidence of resource limitation to aboveground growth of blue grama (Bouteloua gracilis) on 1 ky-old semi-arid substrate

Biogeochemical theory and a substantial body of empirical data show that nitrogen (N), an atmospherically derived nutrient, limits plant growth on young substrates, while phosphorus (P), a rock-derived nutrient, limits plant growth on old substrates. In arid regions, water is also often a limiting resource to plant growth. We applied resource amendments of N, P, N + P, and water to blue grama (Bouteloua gracilis) growing on a 1 ky-old basaltic cinder substrate to test the hypothesis that N and water limit aboveground net primary production (ANPP) in a semi-arid climate, early in soil development. Contrary to our hypothesis, ANPP did not differ among treatments, suggesting that none of the resource amendments were limiting to blue grama growth. Unamended aboveground tissue N and P concentrations were three to five times lower at the 1 ky-old site than on older (55–3000 ky-old) substrates, suggesting differences in nutrient use efficiency across the substrate age gradient.

Proximate controls on semiarid soil greenhouse gas fluxes across 3 million years of soil development

Soils are important sources and sinks of three greenhouse gases (GHGs): carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O). However, it is unknown whether semiarid landscapes are important contributors to global fluxes of these gases, partly because our mechanistic understanding of soil GHG fluxes is largely derived from more humid ecosystems. We designed this study with the objective of identifying the important soil physical and biogeochemical controls on soil GHG fluxes in semiarid soils by observing seasonal changes in soil GHG fluxes across a three million year substrate age gradient in northern Arizona. We also manipulated soil nitrogen (N) and phosphorus availability with 7 years of fertilization and used regression tree analysis to identify drivers of unfertilized and fertilized soil GHG fluxes. Similar to humid ecosystems, soil N2O flux was correlated with changes in N and water availability and soil CO2 efflux was correlated with changes in water availability and temperature. Soil CH4 uptake was greatest in relatively colder and wetter soils. While fertilization had few direct effects on soil CH4 flux, soil nitrate was an important predictor of soil CH4 uptake in unfertilized soils and soil ammonium was an important predictor of soil CH4 uptake in fertilized soil. Like in humid ecosystems, N gas loss via nitrification or denitrification appears to increase with increases in N and water availability during ecosystem development. Our results suggest that, with some exceptions, the drivers of soil GHG fluxes in semiarid ecosystems are often similar to those observed in more humid ecosystems.

Primary Succession on a Hawaiian Dryland Chronosequence.

We used measurements from airborne imaging spectroscopy and LiDAR to quantify the biophysical structure and composition of vegetation on a dryland substrate age gradient in Hawaii. Both vertical stature and species composition changed during primary succession, and reveal a progressive increase in vertical stature on younger substrates followed by a collapse on Pleistocene-aged flows. Tall-stature Metrosideros polymorpha woodlands dominated on the youngest substrates (hundreds of years), and were replaced by the tall-stature endemic tree species Myoporum sandwicense and Sophora chrysophylla on intermediate-aged flows (thousands of years). The oldest substrates (tens of thousands of years) were dominated by the short-stature native shrub Dodonaea viscosa and endemic grass Eragrostis atropioides. We excavated 18 macroscopic charcoal fragments from Pleistocene-aged substrates. Mean radiocarbon age was 2,002 years and ranged from < 200 to 7,730. Genus identities from four fragments indicate that Osteomeles spp. or M. polymorpha once occupied the Pleistocene-aged substrates, but neither of these species is found there today. These findings indicate the existence of fires before humans are known to have occupied the Hawaiian archipelago, and demonstrate that a collapse in vertical stature is prevalent on the oldest substrates. This work contributes to our understanding of prehistoric fires in shaping the trajectory of primary succession in Hawaiian drylands.

Strontium source and depth of uptake shifts with substrate age in semiarid ecosystems

AbstractWithout exogenous rock‐derived nutrient sources, terrestrial ecosystems may eventually regress or reach a terminal steady state, but the degree to which exogenous nutrient sources buffer or slow to a theoretical terminal steady state remains unclear. We used strontium isotope ratios (87Sr/86Sr) as a tracer and measured 87Sr/86Sr values in aeolian dust, soils, and vegetation across a well‐constrained 3 Myr semiarid substrate age gradient to determine (1) whether the contribution of atmospheric sources of rock‐derived nutrients to soil and vegetation pools varied with substrate age and (2) to determine if the depth of uptake varied with substrate age. We found that aeolian‐derived nutrients became increasingly important, contributing as much as 71% to plant‐available soil pools and tree (Pinus edulis) growth during the latter stages of ecosystem development in a semiarid climate. The depth of nutrient uptake increased on older substrates, demonstrating that trees in arid regions can acquire nutrients from greater depths as ecosystem development progresses presumably in response to nutrient depletion in the more weathered surface soils. Our results demonstrate that global and regional aeolian transport of nutrients to local ecosystems is a vital process for ecosystem development in arid regions. Furthermore, these aeolian nutrient inputs contribute to deep soil nutrient pools, which become increasingly important for maintaining plant productivity over long time scales.

Shifting soil resource limitations and ecosystem retrogression across a three million year semi-arid substrate age gradient

The current paradigm of plant nutrient limitation during ecosystem development predicts a change from nitrogen (N) limitation when substrates are young to phosphorus (P) limitation when substrates are old. However, there are surprisingly few direct tests of this model. We evaluated this theory experimentally along a three million year semi-arid substrate age gradient using resource additions to intercanopy spaces dominated by the C4 bunchgrass Bouteloua gracilis. Unlike other gradients in subtropical and temperate ecosystems, soil water availability also increases strongly across this semi-arid system due to finer texture with substrate age. We found that aboveground net primary production (ANPP) of B. gracilis was limited by both water and N on the 55 ky substrate; not limited by N, P, or water on the 750 ky substrate; and limited by P alone on the 3000 ky substrate. Notably, measures of foliar nutrient concentration and N:P mass ratios were unable to predict nutrient limitations in these semi-arid systems. In unamended plots, mean ANPP declined dramatically at 3000 ky compared to the younger substrate age sites, presumably due to progressive limitation by P. This decline in ANPP late in ecosystem development is consistent with a reduction in soil total carbon and N storage at this site and provides a mechanism for successional retrogression in ecosystem structure and function. Our results unify biogeochemical theory across disparate ecosystems while illustrating the important water-nutrient interactions in these semi-arid ecosystems to further define the nature of nutrient limitations in terrestrial ecosystems.

Establishment and growth of piñon pine regeneration vary by nurse type along a soil substrate age gradient in northern Arizona

Future climate predictions suggest that recent patterns of increased piñon pine (Pinus edulis) mortality related to drought in the southwestern U.S. will continue. However, the importance of facilitation for young piñon pine growing at different edaphic sites is not well understood. We measured the density and stem elongation of juvenile piñon pine that established under nurse plants or in open areas in northern Arizona, USA that ranged in soil substrate age from 0.93 to 750ky. We found: 1) 4–9 times greater juvenile piñon pine density under nurse plants compared to open areas; 2) 1–2 times greater densities at the two older substrate sites compared to the younger substrate site; 3) nurse plant effects on juvenile piñon density changed with substrate age; 4) 14–19% greater growth in nursed conditions than open areas across all substrate ages; 5) 32–35% greater growth at the two older substrate age sites; and 6) growth beneath dead piñon nurse plants were approximately 20% greater than under live piñon nurse plants, though differences were not statistically significant (P = 0.07). As a result, we propose that projections of piñon pine distributions need to consider influences of edaphic conditions and the abundance and types of nurse plants on regeneration.

Floristic dynamics across a semi-arid volcanic chronosequence in northern Arizona

Abstract The San Francisco Volcanic Field is one of the dominant volcanic fields on the Colorado Plateau, and its four million-year volcanic history has created a dramatic substrate age gradient. Sites within Pinyon-Juniper woodlands of the volcanic field share similar climate, elevation, and geology yet display dramatically different chemical and structural soil characteristics. The relative degree of soil development associated with ecosystem age strongly influences both the spatial distribution and composition of the local flora. A multiple response permutation procedure indicated that two distinct floristic assemblages occur; one in substrates younger than 150,000 years and one in older substrates. Indicator species analysis revealed that shrubs dominated younger, coarser, poorly developed volcanic soils while grasses and perennial herbs dominated older, finer, more nutrient-rich soils. Younger substrates harbored a higher degree of endemism, and species richness was positively correlated with ecosyst...

Ethylene rather than dissolved organic carbon controls methane uptake in upland soils

Sullivan et al. (2013) reported that there was a significantly positive relationship (P < 0.01, r2 = 0.58) between dissolved organic carbon (DOC) using salt extraction methods and potential methane oxidation rates in an arid region across a substrate age gradient. The authors observed that during the wet season rates of methane oxidation were higher, in opposition to trends in other ecosystems where increased soil moisture limits methane oxidation. Furthermore, DOC was more closely correlated with potential methane oxidation rates than other relevant parameters such as soil moisture content, pore space and texture. After considering alternative options, the authors indicated that DOC may be an important regulator of methane oxidation rates in these arid soils. The authors indicated that this conclusion was supported by observations that incubation with 13C-glucose enriched the methaneoxidizing bacteria (MOB) biomarker 18:1x7c, suggesting that DOC was a facultative substrate for MOB, and also explaining the observed correlation.

The significance of atmospheric nutrient inputs and canopy interception of precipitation during ecosystem development in piñon–juniper woodlands of the southwestern USA

In arid ecosystems, widely spaced vegetation and prolonged dry periods may enhance canopy capture of nutrients from dry deposition. Additionally, differences in precipitation type, plant canopy architecture, and soil nutrient limitation could affect canopy exchange of atmospherically derived nutrients. We collected bulk precipitation and throughfall underneath piñon pine (Pinus edulis) and one-seed juniper (Juniperus monosperma) along a substrate age gradient to determine if canopy interception or throughfall chemistry differed among tree species, season, or substrate age. The Substrate Age Gradient of Arizona consists of four sites with substrate ages ranging from 1 ky to 3000 ky-old, which exhibit classic variations in soil nitrogen (N) and phosphorus (P) availability with substrate age. Greater nutrient inputs below canopies than in intercanopy areas suggest throughfall contributes to the “islands of fertility” effect. Canopy interception of precipitation did not differ between tree species, but was greater in the summer/fall than winter/spring. We found that net canopy retention of atmospherically derived N was generally greater when N availability in the soil was low, but retention also occurred when N availability was relatively high. Taken together, our results were inconclusive in determining whether the degree of soil nutrient limitation alters canopy exchange of plant growth-limiting nutrients.

A positive relationship between the abundance of ammonia oxidizing archaea and natural abundance δ15N of ecosystems

We present a significant relationship between the natural abundance isotopic composition of ecosystem pools and the abundance of a microbial gene. Natural abundance 15N of soils and soil DNA were analysed and compared with archaeal ammonia oxidizer abundance along an elevation gradient in northern Arizona and along a substrate age gradient in Hawai'i. There was a significant positive correlation between the abundance of archaeal amoA genes and natural abundance δ15N of total soil or DNA suggesting that ammonia oxidizing archaea play an important role in ecosystem N release.

Does dissolved organic carbon regulate biological methane oxidation in semiarid soils?

In humid ecosystems, the rate of methane (CH4 ) oxidation by soil-dwelling methane-oxidizing bacteria (MOB) is controlled by soil texture and soil water holding capacity, both of which limit the diffusion of atmospheric CH4 into the soil. However, it remains unclear whether these same mechanisms control CH4 oxidation in more arid soils. This study was designed to measure the proximate controls of potential CH4 oxidation in semiarid soils during different seasons. Using a unique and well-constrained 3-million-year-old semiarid substrate age gradient, we were able to hold state factors constant while exploring the relationship between seasonal potential CH4 oxidation rates and soil texture, soil water holding capacity, and dissolved organic carbon (DOC). We measured unexpectedly higher rates of potential CH4 oxidation in the wet season than the dry season. Although other studies have attributed low CH4 oxidation rates in dry soils to desiccation of MOB, we present several lines of evidence that this may be inaccurate. We found that soil DOC concentration explained CH4 oxidation rates better than soil physical factors that regulate the diffusion of CH4 from the atmosphere into the soil. We show evidence that MOB facultatively incorporated isotopically labeled glucose into their cells, and MOB utilized glucose in a pattern among our study sites that was similar to wet-season CH4 oxidation rates. This evidence suggests that DOC, which is utilized by MOB in other environments with varying effects on CH4 oxidation rates, may be an important regulator of CH4 oxidation rates in semiarid soils. Our collective understanding of the facultative use of DOC by MOB is still in its infancy, but our results suggest it may be an important factor controlling CH4 oxidation in soils from dry ecosystems.

Evaluation of mechanisms controlling the priming of soil carbon along a substrate age gradient

Soil organic matter (SOM) decomposition has the potential to radically affect carbon dioxide concentrations in the atmosphere. Priming, the increased decomposition of SOM after the addition of a labile carbon (C) source, may be an important regulator of SOM dynamics, yet little is known about the mechanisms of the priming effect. Two hypotheses generated in the last decade have suggested that priming is caused by either the nutrient conditions in soil or the response of the microbial community to labile C addition. We used a three million year substrate age gradient, with associated changes in nutrient availability and microbial communities, to test these two hypotheses. We added 13C labeled glucose to soil in quantities similar to increases in root exudation that can be expected in a high carbon dioxide environment, and traced the effect of C addition on soil C, the microbial community, and soil nutrient pools and fluxes. We observed positive priming, negative priming, and no net priming depending on substrate age. Priming was most positive at the youngest sites with the smallest nitrogen (N) pools, and most negative at the site with the most available N. In contrast, we found no significant relationships between priming and phosphorus availability. Though components of the microbial community size and structure (measured by phospholipid fatty acid analysis) changed as a result of C addition, soil N availability was a better explanatory mechanism of priming effects than microbial community dynamics. Our results suggest close linkages between C and N cycles regulate the magnitude and direction of priming. If general, the stability of SOM in temperate ecosystems is likely to be governed by soil N status.

Global nutrient limitation in terrestrial vegetation

Most vegetation is limited in productivity by nutrient availability, but the magnitude of limitation globally is not known. Nutrient limitation is directly relevant not only to ecology and agriculture, but also to the global carbon cycle by regulating how much atmospheric CO2the terrestrial biosphere can sequester. We attempt to identify total nutrient limitation in terrestrial plant productivity globally using ecophysiological theory and new developments in remote sensing for evapotranspiration and plant productivity. Our map of nutrient limitation qualitatively reproduces known regional nutrient gradients (e.g., across Amazonia), highlights differences in nutrient addition to croplands (e.g., between “developed” and “developing” countries), identifies the role of nutrients on the distribution of major biomes (e.g., tree line migration in boreal North America), and compares similarly to a ground‐based test along the Long Substrate Age Gradient in Hawaii, U.S.A. (e.g., foliar and soil nutrients, litter decomposition). Nonetheless, challenges in representing light and water use efficiencies, disturbance, and comparison to ground data with multiple interacting nutrients provide avenues for further progress on refining such a global map. Global average reduction in terrestrial plant productivity was within 16–28%, depending on treatment of disturbance; these values can be compared to global carbon cycle model estimates of carbon uptake reduction with nutrient cycle inclusion.

New evidence that high potential nitrification rates occur in soils during dry seasons: Are microbial communities metabolically active during dry seasons?

Emerging research is challenging existing paradigms of nitrogen (N) cycling in arid and semiarid ecosystems that experience distinct seasonal patterns in precipitation. We measured equal or greater potential nitrification rates in the dry season than the wet season in chemically and physically distinct soils along a three million year substrate age gradient in Arizona. These surprising and counterintuitive results are supported by recently published work in California Mediterranean grasslands. Considered together, these studies call attention to the need to measure process rates during the dry, non-growing season of xeric ecosystems. Several mechanisms may be responsible for these patterns, but we highlight the importance of understanding the contribution of archaeal ammonia oxidizers to nitrification in these seasonally dry ecosystems.

Pinyon pine (Pinus edulis) mortality and response to water addition across a three million year substrate age gradient in northern Arizona, USA

Pinyon pine (Pinus edulis Engelm.) is an important tree species in the western United States that has experienced large-scale mortality during recent severe drought. The influence of soil conditions on pinyon pine response to water availability is poorly understood. We investigated patterns of tree mortality and response of tree water relations and growth to experimental water addition at four sites across a three million year soil-substrate age gradient. We measured recent pinyon mortality at four sites, and tree predawn water potential, leaf carbon isotope signature, and branch, leaf, and stem radial growth on 12 watered and unwatered trees at each site. Watered trees recieved fifty percent more than growing season precipitation for 6 years. Substrate age generally had a greater effect on tree water stress and growth than water additions. Pinyon mortality was higher on intermediate-aged substrates (50–55%) than on young (15%) and old (17%) substrates, and mortality was positively correlated with pinyon abundance prior to drought. These results suggest high soil resource availability and consequent high stand densities at intermediate-age substrates predisposes trees to drought-induced mortality in semi-arid regions. The response of tree water relations to water addition was consistent with the inverse texture hypothesis; watering reduced tree water stress most in young, coarsely textured soil, likely because water rapidly penetrated deep in the soil profile where it was protected from evapotranspiration.

Dependence of Forest Structure and Dynamics on Substrate Age and Ecosystem Development

We quantified rates, sizes, and spatial properties of prevailing disturbance regimes in five tropical rain forest landscapes on a substrate-age gradient in Hawaii. By integrating measurements from airborne LiDAR with field studies and statistical modeling, we show that the structure and dynamics of these forests respond to processes that change during the development of ecosystems. On young substrates of 0.3 ky where forests are in primary succession and are limited by N, mean canopy height was 13 m and height decreases more than 1 m occurred in small, isolated events (power-law exponent = 1.69 ± 0.02, n = 61 gaps ha−1). The proportion of the landscape affected by disturbance increased on high-fertility intermediate-aged substrates of 5–65 ky and canopies were heterogeneous. Frequencies of height decreases more than 1 m were n = 14, 18, and 30 gaps ha−1 corresponding to power-law exponents of 2.188 ± 0.02, 2.220 ± 0.03, and 1.982 ± 0.02 on substrates of 5, 20, and 65 ky. There was a substantial difference between forests on a 150 ky substrate and sites of 5–65 ky; trees on the older substrate formed patchworks of stunted cloud-forest and stands of taller-stature trees. The frequency of recent disturbance events more than 1 m was n = 48 gaps ha−1, corresponding to a power-law exponent of 1.638 ± 0.01. Across the substrate-age gradient, the proportion of each landscape that decreased in height by more than 1 m was 0.16, 0.40, 0.41, 0.36, and 0.17, respectively. These findings demonstrate that substrate age and processes associated with ecosystem development can mediate the rates, sizes, and spatial characteristics of disturbance regimes on forested landscapes, and point toward the necessity of large-area samples to obtain robust estimates of natural dynamics.

Probing carbon flux patterns through soil microbial metabolic networks using parallel position-specific tracer labeling

In order to study controls on metabolic processes in soils, we determined the dynamics of 13CO2 production from two position-specific 13C-labeled pyruvate isotopologues in the presence and absence of glucose, succinate, pine, and legume leaf litter, and under anaerobic conditions. We also compared 13CO2 production in soils along a semiarid substrate age gradient in Arizona. We observed that the C from the carboxyl group (C1) of pyruvate was lost as CO2 much faster than its other C atoms (C2,3). Addition of glucose, pine and legume leaf litter reduced the ratio between 13CO2 production from 1-13C pyruvate and 2,3-13C pyruvate (C1/C2,3 ratio), whereas anaerobic conditions increased this ratio. Young volcanic soils exhibited a lower C1/C2,3 ratio than older volcanic soils. We interpret a low C1/C2,3 ratio as an indication of increased Krebs cycle activity in response to carbon inputs, while the higher ratio implies a reduced Krebs cycle activity in response to anaerobic conditions. Succinate, a gluconeogenic substrate, reduced 13CO2 production from pyruvate to near zero, likely reflecting increased carbohydrate biosynthesis from Krebs cycle intermediates. The difference in 13CO2 production rate from pyruvate isotopologues disappeared 4–5 days after pyruvate addition, indicating that C positions were scrambled by ongoing soil microbial transformations. This work demonstrates that metabolic tracers such as pyruvate can be used to determine qualitative aspects of C flux patterns through metabolic pathways of soil microbial communities. Understanding the controls over metabolic processes in soil may improve our understanding of soil C cycling processes.

Top-Down Analysis of Forest Structure and Biogeochemistry Across Hawaiian Landscapes

Technical and analytical improvements in aircraft-based remote sensing allow synoptic measurements of structural and chemical properties of vegetation across whole landscapes. We used the Carnegie Airborne Observatory, which includes waveform light detection and ranging (LiDAR) and high-fidelity imaging spectroscopy, to evaluate the landscapes surrounding four well-studied sites on a substrate age gradient across the Hawaiian Islands. The airborne measurements yielded variations in ground topography, canopy height, and canopy nitrogen (N) concentration more accurately than they could have been obtained by any reasonable intensity of ground-based sampling. We detected spatial variation in ecosystem properties associated with the properties of different species, including differences in canopy N concentrations associated with the native species Metrosideros polymorpha and Acacia koa, and differences brought about by invasions of the biological N fixer Morella faya. Structural and chemical differences associated with exotic tree plantations and with dominance of forest patches by the native mat-forming fern Dicranopteris linearis also could be analyzed straightforwardly. This approach provides a powerful tool for ecologists seeking to expand from plot-based measurements to landscape-level analyses.