Years Of Ecosystem Development Research Articles

Microbial nutrient limitation along a 2-million-year dune chronosequence

Long-term ecosystem development is characterized by a switch from nitrogen (N) to phosphorus (P) limitation of plant communities as soils age, which leads to changes in plant biomass, diversity, and foliar nutrient concentrations. Similar effects occur belowground, although the extent to which nutrient availability is the primary driver of long-term changes in soil microbial communities remains uncertain. To investigate this, we assessed proxies for soil microbial nutrient limitation along the Jurien Bay dune chronosequence in Western Australia, where a long-term decline in P availability is reflected in strong variation in plant and microbial community composition over 2 million years of soil development. We quantified carbon (C), N, and P in the soil microbial biomass, assayed soil enzymes involved in the acquisition of those nutrients from soil organic matter, and used microbial stoichiometric ratios and vector analysis of enzyme activities to assess whether long-term changes in soil nutrient availability are reflected in nutrient demand by soil microbes. Concentrations of microbial nutrients peaked in Holocene soils (1–6.5 ky), although differences in microbial P were not significant. There were no significant differences in microbial nutrient ratios (C:N, C:P, and N:P) along the chronosequence. Acid phosphatase activity increased continually throughout the chronosequence, while the activities of leucine aminopeptidase and β-glucosidase were greatest in Holocene soils and declined with increasing soil age. Corresponding vector lengths indicated greater investment in C-degrading enzymes in Holocene soils (≤6.5 ky), while vector angles indicated greater investment in the acquisition of P compared with N in Pleistocene soils (≥120 ky). Overall, these findings show that changes in nutrient availability during long-term pedogenesis at Jurien Bay are reflected in microbial investment in nutrient acquisition, but that the soil microbial biomass exhibits a remarkable degree of homeostasis despite major shifts in nutrient availability and community composition over 2 million years of ecosystem development.

Plant footprint decreases the functional diversity of molecules in topsoil organic matter after millions of years of ecosystem development

AbstractAimTheory suggests that the diversity of molecules in soil organic matter (SOM functional diversity) provides key insights on multiple ecosystem services. We aimed to investigate how and why SOM functional diversity and composition change as topsoils develop, and its implications for key soil functions (e.g., from nutrient pool to water regulation).LocationWe reported data on 16 soil chronosequences globally distributed in nine countries from six continents.Time Period2016–2017.Major Taxa StudiedSoil microbes (bacteria and fungi) and vascular plants.MethodsSOM functional diversity and composition without mineral interference were measured using diffuse reflectance mid‐infrared Fourier transform spectroscopy (DRIFT). We aimed to characterize the main environmental factors related to SOM functional diversity and composition. Also, we calculated the links among SOM functional diversity and key soil functions.ResultsWe found that SOM functional diversity declines after millions of years of soil formation (pedogenesis). We further showed that increases in plant cover and productivity led to a higher ratio of reduced (e.g., alkanes) over oxidized carbon forms (i.e., C: O‐functional groups ratio), which was positively correlated to SOM functional diversity as soils age. Our findings indicated that the plant footprint (i.e., the accumulation of plant‐derived material promoting the C: O‐functional group ratio) would explain the reduction of SOM functional diversity as ecosystems develop. Moreover, the dissimilarity in SOM composition consistently increased with soil age, with the soil development stage emerging as the main predictor of SOM dissimilarity across contrasting biomes.Main ConclusionsOur global survey contextualized the natural history of SOM functional diversity and composition during long‐term soil development. Together, we showed how plant footprint drives the losses of SOM functional diversity with increasing age, which might provide a novel mechanism to explain typically reported losses in ecosystem functions during ecosystem retrogression.

Ecological network structure in response to community assembly processes over evolutionary time.

The dynamic structure of ecological communities results from interactions among taxa that change with shifts in species composition in space and time. However, our ability to study the interplay of ecological and evolutionary processes on community assembly remains relatively unexplored due to the difficulty of measuring community structure over long temporal scales. Here, we made use of a geological chronosequence across the Hawaiian Islands, representing 50 years to 4.15million years of ecosystem development, to sample 11 communities of arthropods and their associated plant taxa using semiquantitative DNA metabarcoding. We then examined how ecological communities changed with community age by calculating quantitative network statistics for bipartite networks of arthropod-plant associations. The average number of interactions per species (linkage density), ratio of plant to arthropod species (vulnerability) and uniformity of energy flow (interaction evenness) increased significantly in concert with community age. The index of specialization has a curvilinear relationship with community age. Our analyses suggest that younger communities are characterized by fewer but stronger interactions, while biotic associations become more even and diverse as communities mature. These shifts in structure became especially prominent on East Maui (~0.5million years old) and older volcanos, after enough time had elapsed for adaptation and specialization to act on populations in situ. Such natural progression of specialization during community assembly is probably impeded by the rapid infiltration of non-native species, with special risk to younger or more recently disturbed communities that are composed of fewer specialized relationships.

Soil potassium isotope composition during four million years of ecosystem development in Hawai‘i

We combine spectroscopic and geochemical approaches to interpret the fate of potassium (K) during forest soil development along a 4-million-year chronosequence sampled from relatively undisturbed rainforests in Hawai‘i. Potassium derived from weathering of lava is dominant in the youngest site (0.3 ky), but its contribution to the soil K budget declines as weathering progresses. Sites older than 0.3 ky are characterized by substantial K depletion (τK,Nb ∼−1), with soil isotopic composition (41K/39K, δ41K) varying from −1.91 ± 0.08‰ to −0.09 ± 0.08‰, relative to the homogeneous basaltic substrate (−0.48‰). Exchangeable and interlayered K show δ41K values ranging from −1.32 ± 0.06‰ to 0.06 ± 0.08‰, higher than their corresponding bulk δ41K values. The δ41K patterns of soils and exchangeable components are vertically similar, implying similar environmental controls. The variability in K phase and isotope composition reflects the accumulative effect of different processes. Chemical weathering and plant cycling retain isotopically light K in soils, in particular for 20–150 ky sites. In contrast, atmospheric inputs of marine aerosols (0.14‰) and mineral aerosols (−0.44‰) add heavier K (than native basalts) and crust-like K (similar to basaltic δ41K) in soils, respectively. In sites older than 150 ky, nearly complete depletion of basaltic K and reduced plant K imprints result in the dominance of atmospheric inputs in soils. In sum, this study emphasizes the sensitivity of δ41K to terrestrial biotic and abiotic K cycles.

The evolution of stream dissolved organic matter composition following glacier retreat in coastal watersheds of southeast Alaska

Climate change is melting glaciers and altering watershed biogeochemistry across the globe, particularly in regions dominated by mountain glaciers, such as southeast Alaska. Glacier dominated watersheds exhibit distinct dissolved organic matter (DOM) characteristics compared to forested and vegetated watersheds. However, there is a paucity of information on how stream DOM composition changes as glaciers retreat and terrestrial ecosystem succession ensues. Importantly, it is unclear over what timescales these transformations occur. Here, we used bulk, isotopic and ultrahigh resolution molecular-level techniques to assess how streamwater DOM composition evolves in response to glacier retreat and subsequent terrestrial ecosystem succession. For this, water samples were collected from eleven streams across a chronosequence spanning a temporal gradient 0 to ~ 1400 years since glacier retreat in coastal, southeast Alaska. During the first ~ 200 years since glacier retreat, stream DOM showed marked and consistent changes in bulk, isotopic, and molecular-level composition. In particular, there was a decreased relative abundance (RA) of ancient, energy-rich (e.g., elevated aliphatic contribution), low aromaticity (e.g., low SUVA254 and AImod) DOM and an increased RA of soil and vegetation derived aromatic DOM (e.g., more depleted δ13C, elevated condensed aromatic and polyphenolic contribution) that had a modern radiocarbon age. After ~ 200 years of ecosystem development, DOM composition was comparable to that observed for other temperate and arctic forested watersheds without permafrost influence. These results underscore the timelines on which glacier retreat may have substantial impacts on watershed biogeochemistry and coastal ecosystems that receive DOM from these rapidly changing landscapes.

High sulfate concentrations maintain low methane emissions at a constructed fen over the first seven years of ecosystem development

Wetlands comprise a large expanse of the pre-disturbance landscape in the Athabasca Oil Sands Region (AOSR) and have become a focus of reclamation in recent years. An important aspect of wetland reclamation is understanding the biogeochemical functioning and carbon exchange, including methane (CH4) emissions, in the developing ecosystem. This study investigates the drivers of CH4 emissions over the first seven years of ecosystem development at a constructed fen in the AOSR and looks towards future CH4 emissions from this site. Specifically, the objectives were to: 1) investigate the environmental controls on CH4 emissions measured using manual static chambers between 2013 and 2019 and 2) investigate the relationship between water table depth, sulfate (SO42−) concentrations and CH4 emissions during the 2019 growing season. Methane emissions remained low throughout the majority of the measurement period; however, in later years, a small but significant increase became apparent. High levels of SO42− are likely the cause of the low CH4 emissions, despite the high-water tables and dominance of vegetation with aerenchyma such as Carex aquatilis and Typha latifolia in later years. Although low CH4 emissions may be beneficial from a climate warming perspective, the results also suggest that this constructed peatland is not functioning similarly to regional reference fens. Future climate scenarios across Western Boreal Canada could lead to higher air temperatures and changing precipitation patterns, influencing the direction of future CH4 emissions from this site. However, given the likelihood of this site maintaining extremely high SO42− concentrations over the next decade, it is expected that CH4 emissions will remain low.

Soil microbial communities influencing organic phosphorus mineralization in a coastal dune chronosequence in New Zealand.

The Haast chronosequence in New Zealand is an ∼6500-year dune formation series, characterized by rapid podzol development, phosphorus (P) depletion and a decline in aboveground biomass. We examined bacterial and fungal community composition within mineral soil fractions using amplicon-based high-throughput sequencing (Illumina MiSeq). We targeted bacterial non-specific acid (class A, phoN/phoC) and alkaline (phoD) phosphomonoesterase genes and quantified specific genes and transcripts using real-time PCR. Soil bacterial diversity was greatest after 4000 years of ecosystem development and associated with an increased richness of phylotypes and a significant decline in previously dominant taxa (Firmicutes and Proteobacteria). Soil fungal communities transitioned from predominantly Basidiomycota to Ascomycota along the chronosequence and were most diverse in 290- to 392-year-old soils, coinciding with maximum tree basal area and organic P accumulation. The Bacteria:Fungi ratio decreased amid a competitive and interconnected soil community as determined by network analysis. Overall, soil microbial communities were associated with soil changes and declining P throughout pedogenesis and ecosystem succession. We identified an increased dependence on organic P mineralization, as found by the profiled acid phosphatase genes, soil acid phosphatase activity and function inference from predicted metagenomes (PICRUSt2).

Plant-soil feedbacks on free-living nitrogen fixation over geological time.

Free-living heterotrophic nitrogen fixation (FNF) is a widespread nitrogen input pathway in terrestrial ecosystems. However, questions remain over the relative influence of co-occurring controls on patterns of heterotrophic FNF activity, especially across generalized stages of primary succession, from biomass accumulation to retrogressive phases. Here, we experimentally test two alternative hypotheses regarding FNF rates during ecosystem development: (H1) site (i.e., changes in soil fertility during succession) is the primary driver of leaf-litter FNF rates, vs. (H2) leaf-litter chemistry is the primary determinant of FNF activity across a broad range of ecosystem conditions. We evaluated these hypotheses across a well-studied soil chronosequence in California (i.e., the Ecological Staircase), which spans ~1million years of ecosystem development and displays extreme ranges in plant-soil nutrient conditions, culminating in the nutrient depleted and stunted Pygmy forest. Across this successional gradient, we implemented a reciprocal leaf-litter transplant and a common garden litter bag decomposition experiment with senesced needles of Pinus muricata. Our results support H1: rates of FNF were similar for all leaf-litter types decomposed at the same site regardless of initial leaf-litter C and nutrient contents. FNF rates sharply declined from the maximal to retrogressive stage of succession. Trends in P dynamics during decomposition suggest an important role of P in regulating FNF. For example, P.muricata litter collected from the infertile Pygmy site displayed substantially higher FNF rates when decomposed at the fertile site, in part by immobilizing significant quantities of P from the soil at the fertile site. Conversely, P.muricata litter collected from the fertile site decomposed more slowly at the Pygmy site, with concomitant declines in FNF rates that matched those of Pygmy site litter decomposed insitu. These results are consistent with the idea that, over millennia, long-term declines in P availability feedback to constrain FNF rates, in part explaining the emergence of extremely nutrient-poor and retrograded ecosystems.

Decreased occurrence of carbon cycle functions in microbial communities along with long-term secondary succession

The succession of microbial community structure and function is a central ecological topic; however, the mechanisms that underlie community assembly and promote temporal succession remain unclear. We studied microbial community-associated functional dynamics in a well-established secondary successional chronosequence that spans approximately 160 years of ecosystem development on the Loess Plateau of China, by sequencing both 16S and ITS rRNA genes and soil metagenomes, resulting in a total of 132.5 Gb of data. Notably, both bacterial and fungal communities shifted with succession, but the microbial community changed little from the pioneer forest stage (approximately 110 years) to the latter successional forest stage. Fungi showed higher variability with succession than bacteria, and the shift of both the bacterial and fungal communities was related more to the soil characteristics than to the litter characteristics. Shifts in soil microbial functions were associated with microbial phylogenetic changes, but microbial gene function also showed changes in the absence of phylogenetic changes at the late successional stages. The reduction in microbial C cycle genes was related to a decrease in litter decomposition ability, thus resulting in a steady state of nutrient cycle in the ecosystem. In addition, high microbial respiration in nutrient-rich soil does not necessarily indicate high microbial decomposition functions; the latter also depend on the abundance of related genes, on enzyme activity and on the physicochemical properties of the litter. Our study provides a metagenome profile of a successional chronosequence and provides insight into the mechanisms underlying the soil microbe-driven functional changes in nutrient cycles during succession.

Research Article: Soil respiration in upper Great Lakes old-growth forest ecosystems

Forests, through photosynthetic fixation of carbon dioxide, serve as natural carbon (C) sinks, thereby offsetting a substantial fraction of anthropogenic greenhouse gas emissions. However, forests of the upper Great Lakes region are on average getting older, prompting uncertainty in the region's future capacity to sequester C. Several studies demonstrate higher-than-expected rates of C sequestration in biomass and soils, or net ecosystem production (NEP), of older forests, with declining C losses from soils a proposed mechanism sustaining NEP as forests age. Forest plots spanning nearly 200 years of ecosystem development and including three different old-growth forest types were used to examine changes with age in growing season soil respiration (Rs) - the C emitted from soils by roots and soil microbes. How heterotrophic soil respiration (Rh) - the C emitted from soils by microbes only - varies among old-growth forest types and with soil environment was also examined. Mean growing season Rs and soil temperature were significantly lower in old-growth forests, with the former declining as forests aged. Laboratory incubations and scaled estimates of Rh suggest significantly higher rates in more tree species diverse mixed canopy old-growth forests than in less diverse conifer and deciduous old-growth forest stands. Soil moisture was an important driver of Rh in all old-growth forest types, particularly in the top, carbon-rich organic horizon. Based on the results of this study, it can be concluded that declining C emissions from the soils of old-growth forests may contribute to unexpectedly high rates of forest C sequestration as forests age.

Microbial community succession and bacterial diversity in soils during 77 000 years of ecosystem development

The origins of the biological complexity and the factors that regulate the development of community composition, diversity and richness in soil remain largely unknown. To gain a better understanding of how bacterial communities change during soil ecosystem development, their composition and diversity in soils that developed over c. 77 000 years of intermittent aeolian deposition were studied. 16S rRNA gene clone libraries and fatty acid methyl ester (FAME) analyses were used to assess the diversity and composition of the communities. The bacterial community composition changed with soil age, and the overall diversity, richness and evenness of the communities increased as the soil habitat matured. When analysed using a multivariate Bray-Curtis ordination technique, the distribution of ribotypes showed an orderly pattern of bacterial community development that was clearly associated with soil and ecosystem development. Similarly, changes in the composition of the FAMEs across the chronosequence were associated with biomarkers for fungi, actinomycetes and Gram-positive bacteria. The development of the soil ecosystem promoted the development of distinctive microbial communities that were reminiscent of successional processes often evoked to describe change during the development of plant communities in terrestrial ecosystems.

15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function

Organic carbon (C) and nitrogen (N) are essential for heterotrophic soil microorganisms, and their bioavailability strongly influences ecosystem C and N cycling. We show here that the natural (15)N abundance of the soil microbial biomass is affected by both the availability of C and N and ecosystem N processing. Microbial (15)N enrichment correlated negatively with the C : N ratio of the soil soluble fraction and positively with net N mineralization for ecosystems spanning semiarid, temperate and tropical climates, grassland and forests, and over four million years of ecosystem development. In addition, during soil incubation, large increases in microbial (15)N enrichment corresponded to high net N mineralization rates. These results support the idea that the N isotope composition of an organism is determined by the balance between N assimilation and dissimilation. Thus, (15)N enrichment of the soil microbial biomass integrates the effects of C and N availability on microbial metabolism and ecosystem processes.

Erosion and landscape development affect plant nutrient status in the Hawaiian Islands

We quantified variation in plant nutrient concentrations and provenance along catenas in landscapes of three different ages (0.15, 1.4, and 4.1 ma) in the Hawaiian Islands. Strontium (Sr) isotopes demonstrate that erosion provides a renewed source of rock-derived nutrients to slopes in landscapes of all ages, in some cases reversing a million years of ecosystem development in a distance of 100 m. However the effects of this input vary with landscape age. Plants on uneroded surfaces in a 0.15-ma landscape derive approximately 20% of their Sr from local bedrock (foliar 87Sr/86Sr approximately 0.7085), while on adjacent slopes this increases to approximately 80% (foliar 87Sr/86Sr approximately 0.7045). Despite this shift in provenance, foliar N and P do not vary systematically with slope position. Conversely, eroded slopes in a 4.1-ma landscape show smaller increases in rock-derived cations relative to stable uplands (foliar 87Sr/86Sr approximately 0.7075 vs 0.7090), but have >50% higher foliar N and P. These results demonstrate both that erosion can greatly increase nutrient availability in older landscapes, and that the ecological effects of erosion vary with landscape age. In addition, there can be as much biogeochemical variation on fine spatial scales in eroding landscapes as there is across millions of years of ecosystem development on stable surfaces.

Changing sources of nutrients during four million years of ecosystem development

As soils develop in humid environments, rock-derived elements are gradually lost, and under constant conditions it seems that ecosystems should reach a state of profound and irreversible nutrient depletion. We show here that inputs of elements from the atmosphere can sustain the productivity of Hawaiian rainforests on highly weathered soils. Cations are supplied in marine aerosols and phosphorus is deposited in dust from central Asia, which is over 6,000 km away.