Browsing by Author "Jackson, Robert B"

Plants respond to changes in their local environment and, at the same time, influence the environment at a global scale. The molecular and physiological mechanisms regulating this interaction are not completely understood and this limits our capacity to predict the response of vegetation to future environmental changes. This dissertation combined tools from genomics, physiology, and ecology to examine the response of plants to environmental change. Specifically, it focused on processes affecting carbon and water exchange in forest trees because (1) trees are long-lived species that might face repeated environmental challenges; (2) relatively little information exists about the genes and the molecular mechanisms regulating structural and physiological traits in adult, long-lived woody plants; and (3) forest trees exchange a significant amount of carbon and water with the atmosphere and are therefore major players in the global carbon and water cycles.

Water flux through forests depends both on environmental conditions (e.g., soil moisture) and on the hydraulic architecture of individual trees. Resistance to xylem cavitation is an important hydraulic trait that is often associated with drought tolerance but potentially at the cost of reduced carbon uptake. The second chapter of this dissertation evaluated the variation in resistance to xylem cavitation, hydraulic conductivity, wood anatomy traits, and leaf gas exchange across 14 co-occurring temperate tree species including both angiosperms and gymnosperms. The relationship between vulnerability to cavitation (ψ₅₀) and hydraulic conductivity within specific organs (i.e. stems and roots) was not significant when considering the phylogenetic association between species. However, even after phylogenetic correction, photosynthetic carbon uptake (A) was positively correlated with both stem and root ψ₅₀, and stomatal conductance (g_s ) was strongly correlated with root ψ₅₀ . These results suggest that there is a trade-off between vulnerability to cavitation and water transport capacity at the whole-plant level, and that this functional relationship reflects an adaptive response to the environment.

Forests are an important component of the global carbon cycle that can be directly impacted by a rise in atmospheric CO₂ concentration.. The third chapter of this dissertation investigated the effects of long-term exposure to elevated CO2 on the gene expression of mature, field-grown loblolly pine trees. Using cDNA microarrays, I compared the expression of 1784 pine transcripts in trees growing under ambient and those under elevated CO₂ at monthly intervals throughout a growing season. Overall, more genes were upregulated than downregulated by elevated CO₂, although the total number of genes differentially expressed varied throughout the season. The pattern of increasing number of differentially expressed genes until the peak of the growing season (July and August) followed by a decrease in that number, matched the seasonal trend of tree growth and photosynthetic response to elevated CO₂ in this species. The seasonal trend also reflected the interaction among multiple abiotic factors intrinsic to field conditions and emphasized the relevance of evaluating the role of genes in their natural environment. Genes consistently upregulated by elevated CO₂ were functionally associated with environmental sensing, cellular signaling, and carbon metabolism, in particular the degradation of carbohydrates through respiration. An increase in carbohydrates degradation is particularly relevant in the context of carbon balance of forest trees because of the potential for enhanced leaf and tree respiration leading to a reduced sink capacity for CO₂.

Loblolly pine produces several flushes of needles throughout the year each with an average lifespan of 19 months. Each year, two age classes of needles contribute to the annual carbon sequestration of the loblolly pine forest. To address the impact of leaf age on the effects of elevated CO₂ in carbon metabolism regulation, I compared the gene expression profiles from trees under ambient and elevated CO₂ conditions in two needle cohorts: one-year-old and current-year. Differential expression under elevated CO₂ was seven times more frequent in current-year than in one-year-old needles. Despite differences in magnitude, many of the patterns within specific groups of genes were similar across age classes. For instance, there was a trend for downregulation of genes involved in the light-reactions of photosynthesis and those in photorespiration in both age classes, while genes associated with dark respiration were largely upregulated by elevated CO₂ in both cases. The difference between the two cohorts was particularly evident in the group of genes related to energy production (ATP synthesis) and the group associated with carbon partitioning (sucrose and starch metabolism). Because sucrose and starch metabolism categories included many genes known to be important regulators of gene expression and plant physiological processes, this suggests that this stage of carbon metabolism might be an important control point in age-dependent foliar responses to elevated CO₂.

This dissertation examined both structural and physiological components of plant water and carbon relations (Chapter 2) across different biological scales of organization (whole-plant level in Chapter 2; gene-level response to ecosystem-level changes in Chapters 3 and 4) and reflecting adjustments at distinct temporal scales (life-span of the organism vs. evolutionary selection of traits). An integrative approach was used to advance our understanding of how plants acclimate and adapt to their environment, and to provide a mechanistic framework for predictive models of plant response to environmental change.

Rivers interact with their valleys from headwaters to mouth, but nowhere as dynamically as in their floodplains. Rivers deliver water, sediments, and solutes onto the floodplain land surface, and the land in turn supplies solutes, leaves, and woody debris to the channel. These reciprocal exchanges maintain both aquatic and terrestrial biodiversity and productivity. In this dissertation I examine river-floodplain exchanges on the well-studied Nyack Floodplain, a dynamic, gravel-bedded floodplain along the Middle Fork Flathead River in the mountains of northwest Montana. I quantify exchanges at multiple timescales, from moments to centuries, to better understand how connectivity between aquatic and terrestrial habitats shapes their ecology.

I first address connectivity in the context of a long-standing question in ecosystem ecology: What determines the rate of ecosystem development during primary succession? Rivers have an immediate effect on floodplains when scouring floods remove vegetation and nutrients such as nitrogen (N) and leave only barren soils, but they might also affect the ensuing primary succession through the gradual delivery of N and other materials to floodplain soils. I quantify N inputs to successional floodplain forest soils of the Nyack Floodplain and find that sediment deposition by river flood water is the dominant source of N to soils, with lesser contributions from dissolved N in the river, biological N fixation, and atmospheric deposition. I also synthesize published rates of soil N accumulation in floodplain and non-floodplain primary-successional systems around the world, and I find that western floodplains often accumulate soil N faster than non-floodplain primary successional systems. My results collectively point to the importance of riverine N inputs in accelerating ecosystem development during floodplain primary succession.

I next investigate the role of river-floodplain exchanges in shaping the spatial distribution of a suite of soil properties. Even after flood waters have receded, dissolved N, carbon (C), and moisture could be delivered from the river to floodplain soils via belowground water flow. Alternatively, C inputs and N withdrawals by floodplain vegetation might be a dominant influence on soil properties. To test these hypotheses, I excavated and sampled soil pits from the soil surface to the water table (50-270 cm) under forests, meadows, and gravel bars of the Nyack Floodplain. Near-surface soils had C and N pools and N flux rates that varied predictably with vegetation cover, but soil properties below ~50 cm reflected influence by neither vegetation cover nor aquifer delivery. Instead, soil properties at these depths appear to relate to soil texture, which in turn is structured by the river's erosional and depositional activities. This finding suggests the revised hypothesis that soil properties in gravel-bedded alluvial floodplains may depend more on the decadal-scale geomorphic influences of floods than on short-term vertical interactions with floodplain vegetation or aquifer water.

Lastly, I explore the potential sources of organic C to the diverse and active community of aquatic organisms in the floodplain aquifer, where the lack of light prohibits in-situ organic C production by photosynthesis. I quantify floodplain carbon pools and the fluxes of organic carbon connecting the aquifer, river, and overlying forest. Spring flood waters infiltrating the soil are responsible for the largest dissolved carbon flux into the aquifer, while very large floods are essential for the other major C input, the burial of woody carbon in the aquifer. These findings emphasize the importance of a dynamic river hydrograph - in particular, annual floods and extreme annual floods - in delivering organic C to the aquifer community.

Overall, this dissertation draws our attention not just to the current exchanges of C, N, water, and sediment but to the episodic nature of those exchanges. To fully understand floodplain ecosystems, we have to consider not just present-day interactions but also the legacies of past floods and their roles in delivering solutes, eroding forests, depositing sediments, and physically shaping the floodplain environment.

Rising atmospheric CO2 concentration, currently about 390 ppm, causes climate change and is expected to reach 500 ppm or higher this century due to human activities. Soils are the largest terrestrial pool of carbon, and changes in soil carbon storage due to plant and microbial activities could affect atmospheric CO2 levels. This dissertation studies soil carbon and microbial responses to an experimental preindustrial-to-future CO2 gradient (250-515 ppm) in a grassland ecosystem. Two contrasting soil types are studied in the gradient, providing insight on how natural ecosystem variation modifies CO2 effects.

Although total soil organic carbon (SOC) did not change with CO2 treatment after four growing seasons, fast-cycling SOC pools did respond to CO2, particularly in the black clay soil. Microbial biomass increased 18% and microbial activity increased 30% across the CO2 gradient in the black clay, but neither factor changed with CO2 in the sandy loam. Similarly a one-year laboratory soil incubation showed that a fast-cycling SOC pool increased 75% across the CO2 gradient in the black clay. Size fractionation of SOC showed that coarse POM-C, the youngest and most labile fraction, increased four-fold across the CO2 gradient in the black clay, while it increased 50% across the gradient in the sandy loam. CO2 enrichment in this grassland increased the fast-cycling soil organic carbon pool as in other elevated CO2 studies, but only in the black clay soil.

CO2 also induced changes in microbial community composition, and we explored the functional consequences in a microcosm experiment. Soil collected in the third growing season of CO2 treatment was used to inoculate Indiangrass seedlings grown in the lab. The elevated CO2 soil inoculum had higher microbial biomass C/N (C/N = 21) than the subambient CO2 soil inoculum (C/N = 16), suggesting a difference in community composition. Mean plant height in elevated CO2 soil inoculum (475 ppm) was 57% greater than in subambient CO2 soil inoculum (300 ppm), but the difference was not statistically significant. Similarly, total leaf N from plants in elevated CO2 soil was 28% greater on average than in subambient CO2 soil, but not significantly different. CO2-induced microbial effects on plant growth were either negligible or occurred at finer microbial taxonomic levels, making them difficult to resolve at the whole-community level.

Soil fungi decompose soil organic matter, and studying fungal community responses to CO2 could improve our understanding of soil carbon responses. We studied fungal communities in the CO2 gradient using Sanger sequencing and pyrosequencing of rDNA. As in our soil C study, fungal community responses to CO2 were mostly linear, and occurred mostly in the black clay soil. Fungal species richness increased linearly with CO2 treatment in the black clay. The relative abundance of Chytridiomycota (chytrids) increased linearly with CO2 in the black clay, while the relative abundance of Glomeromycota (arbuscular mycorrhizal fungi) increased linearly with CO2 in the sandy loam. Increased labile C availability at elevated CO2 and/or decreased inorganic N may explain the increase in fungal species richness and Chytridiomycota abundance in the black clay, while increased P limitation may explain the stimulation of Glomeromycota at elevated CO2 in the sandy loam. Across both soils, fungal species richness increased linearly with soil respiration, an index of decomposition rate (p = 0.01, R2 = 0.46). Adding fungal species may have improved decomposition efficiency, but it is also possible that species richness and decomposition increased due to another factor such as C quantity. Soil type strongly structured both fungal community and arbuscular mycorrhizal fungal community composition.

Together, these studies suggest that soil C and fungal community responses to CO2 were mostly linear, and were most apparent in the black clay soil. Soil type strongly influenced fungal community composition as well as which phyla responded to CO2. Therefore, soil type could be a useful addition to predictions of soil carbon and microbial responses to future CO2 levels.

Root carbon exudation is a critical element of the soil carbon cycle, and how both environmental conditions and plant traits influence exudation remains uncertain. I studied relationships between environmental conditions, plant traits, and carbon exudation in four herbaceous plant species: Asclepias incarnata, Microstegium vimineum, Panicum virgatum, and Scirpus cyperinus. Mature individuals were given short-term factorial light and N treatments, and exudates were collected from 8-hour carbon-free hydroponic incubations. I measured size traits (biomass, leaf area, root length, and root volume), photosynthesis (leaf-level and whole-plant), and tissue N traits (root, stem, and leaf percent N and C:N ratio). Neither light nor N treatments affected exudation, while exudation varied with species and traits. Species alone substantially explained mass-specific exudation (estimated R2 = 0.38). Size strongly predicted both total and mass-specific exudation, interacting with species (estimated R2 = 0.52 and 0.48, respectively). Generally, larger individuals exuded more overall but less per unit mass, although larger M. vimineum plants exuded more per unit mass. Whole-plant photosynthetic rate was weakly related to total exudation (estimated R2 = 0.17), and tissue N concentration moderately predicted mass-specific exudation (estimated R2 = 0.23). Other researchers have found that high light and low nitrogen availability stimulate exudation; my results indicate that this relationship is not straightforward. Plant traits, however, significantly explained variation in exudation, including some variation across species, supporting trait-based analyses of plant species' effects on ecosystem processes.

Methane is an important greenhouse gas, and an ideal target for greenhouse gas emissions reductions. Unlike carbon dioxide, methane has a relatively short atmospheric lifetime, so reductions in methane emissions could have large and immediate impacts on anthropogenic radiative forcing. A more detailed understanding of the global methane budget could help guide effective emissions reductions efforts.

Humans have greatly altered the methane budget. Anthropogenic methane sources are approximately equal in flux to natural sources, and the current atmospheric methane concentration is ~2.5 times pre-industrial levels. The advent of hydraulic fracturing and resulting increase in unconventional natural gas extraction have introduced new uncertainties in the methane budget. At the same time, the next few decades could be a crucial period for controlling greenhouse gas emissions to avoid irreversible and catastrophic changes in global climate. Natural gas could provide lower-carbon fossil energy, but the climate benefits of this fuel source are highly dependent on the associated methane emissions. In this context of increasing uncertainty and growing necessity, quantifying the impact of natural gas extraction and use on the methane budget is an essential step in making informed decisions about energy.

In the work presented here, I track methane in the environment to address several areas of uncertainty in our present understanding of the methane budget. I apply the tools of methane analysis in a variety of environments, from rural groundwater supplies to an urban atmosphere, and at a range of scales, from individual point sources to regional flux. I first show that carbon isotopes of methane and co-occurrence of ethane are useful techniques for differentiating a range of methane sources. In so doing, I also show that leaks from natural gas infrastructure are a major source of methane in my study area, Boston, MA. I then build on this work by applying the same methane carbon isotope and ethane signatures to partition methane flux for the Boston metro region. I find that 88% of the methane enhancement in the atmosphere above Boston is due to pipeline natural gas.

In the final portion of this thesis and the two appendices, I move from the distribution side of the natural gas production chain to extraction, specifically addressing the potential impacts from hydraulic fracturing in my home state of North Carolina. I combine the methane source identification techniques of the previous sections with additional geochemical analyses to document the pre-drilling water quality in the Deep River Triassic Basin, an area which could be drilled for natural gas in the future. This data set is unique in that North Carolina has no pre-existing commercial oil and gas extraction, unlike other states where unconventional gas extraction is currently taking place. This research is, to my knowledge, the first to examine the hydrogeology of the Deep River Basin, in addition to providing an important background data set that could be used to track changes in water quality accompanying hydraulic fracturing in the region in the future.

Afforestation, the conversion of historically treeless areas into forests, is a rapidly spreading land-use change with the potential to sequester carbon. Afforested plantations typically feature fast growing exotic tree species that give landowners rapid returns. The efficient growth of plantations compared to less intensively managed forests also can provide greater timber yields in a smaller area. This increased efficiency in turn could require fewer acres to meet global forest product demands and could also reduce the need to log intact primary forests. Reduced primary forest harvest and high primary productivity make afforestation a highly efficient carbon sequestration tool.

However, the rapid growth and planting disturbance due to afforestation can have deleterious effects on soils and hydrology that undermine its benefits in some locations. The effects on hydrology include depletion of groundwater and reduced or complete elimination of surface water flow. Additionally, groundwater use can lead to increased concentrations of salts and trace metals in soil that could be deleterious for future plant productivity. Plantations have also been shown to acidify surface soils and stream water and to reduce soil carbon and nitrogen.

Despite the known effects of afforestation on soils, there has been little research on the mechanisms controlling these effects. For instance, there have been few studies on the effects of afforestation on soil microbes which mediate most biogeochemical processes. There is also little knowledge on what controls the effects of afforestation on soil carbon and nitrogen, vital indexes of soil quality, across regions with high levels of afforestation. The overarching goal of this dissertation is to examine the effects of afforestation on soils, microbes, and biogeochemical processes across local, regional and global scales. Understanding the mechanisms by which afforestation alters soils and biogeochemical cycling and how these mechanisms change across different scales will aid in evaluating the true costs and benefits of afforestation. These results will be useful in determining if the benefits of afforestation will continue to outweigh its costs in the long-term.

The goal of Chapter 1 is to evaluate how afforestation across the globe affects mineral soil quality, including pH, sodium, exchangeable cations, organic carbon, and nitrogen, and to examine the magnitude of these changes in regions where afforestation rates are high. To control for different initial soil conditions across the globe, I examined paired sites of afforested plantations and controls. Controls included land-use types that are frequently afforested, such as grasslands, shrublands, and pastures. I also examined potential mechanisms to reduce the impacts of afforestation on soils and to maintain long-term productivity. Across diverse plantation types (153 sites) to a depth of 30cm of mineral soil, I observed significant decreases in nutrient cations (Ca, K, Mg), increases in sodium (Na), or both with afforestation. For the global dataset, afforestation reduced soil concentrations of the macronutrient Ca by 29% on average compared with native controls (p<0.05). Afforestation by Pinus alone decreased soil K by 23% (p<0.05). Overall, plantations of all genera also led to an average 71% increase of soil Na (p<0.05). Average pH decreased 0.3 units (p<0.05) with afforestation. Afforestation caused a 6.7% and 15% (p<0.05) decrease in soil C and N content respectively, though the effect was driven principally by Pinus plantations (15% and 20% decrease, p<0.05). Carbon to nitrogen ratios in soils under plantations were 5.7-11.6% higher (p<0.05). The major implication of these results are that in several regions with high rates of afforestation, cumulative losses of C, N, Ca, and Mg are likely in the range of tens of millions of metric tons. The decreases indicate that trees take up considerable amounts of nutrients from soils; harvesting this biomass repeatedly could impair long-term soil fertility and productivity in some locations. Based on this study and a review of other literature, I suggest that proper site preparation and sustainable harvest practices, such as avoiding the removal or burning of harvest residue, could minimize the impact of afforestation on soils. These sustainable practices could in turn slow erosion, organic matter loss, and soil compaction from harvesting equipment, maintaining soil fertility to the greatest extent possible.

Soil microbes are highly diverse and control most soil biogeochemical reactions. Given the observed changes in Chapter 1, in Chapters 2 and 3 I examined how microbial functional genes and biogeochemical pools responded to the altered chemical inputs accompanying afforestation. I examined paired native grasslands and adjacent Eucalyptus plantations (previously grasslands) in Uruguay, a region that lacked forests before European settlement. Along with measurements of soil carbon, nitrogen, and bacterial diversity, I analyzed functional genes using the GeoChip 2.0 microarray that simultaneously quantified several thousand genes involved in soil carbon and nitrogen cycling. Plantations and grasslands differed significantly in functional gene profiles, bacterial diversity, and biogeochemical pool sizes. Afforestation decreased both bacterial diversity and richness compared to grasslands, though diversity remained relatively high. Most grassland functional gene profiles were similar, but plantation profiles generally differed from grasslands due to differences in functional gene abundance across many microbial groups. Eucalypts decreased ammonification and N-fixation functional genes by 11% and 7.9% (p<0.01) which correlated with decreased microbial biomass N and more NH4+ in plantation soils. Chitinase, an important carbon polymer degrading enzyme, decreased in functional gene abundance 7.8% in plantations compared to grasslands (p=0.017), and C polymer degrading genes decreased by 1.5% overall (p<0.05), which likely contributed to 54% (p<0.05) more C in undecomposed extractable soil pools and 27% less microbial C (p<0.01) in plantation soils. In general, afforestation altered the abundance of many microbial functional genes corresponding with changes in soil biogeochemistry. These changes were driven by shifts in the whole community functional gene profile, not just one or two constituent microbial taxa. Such changes in microbial functional genes correspond with altered C and N storage and have implications for long-term productivity in these soils.

The area studied in Chapters 2 and 3 lies near the middle of a precipitation gradient that stretches across the Rio de la Plata grasslands. In Chapter 4 I studied if the effects of afforestation on soil C and N from Chapters 2 and 3 varied with different precipitation levels. The effect of afforestation on soil C has been shown to depend on mean annual precipitation (MAP), with drier sites gaining C and wetter sites losing C with afforestation. This precipitation dependence of soil C changes with afforestation may be controlled by changes in soil nitrogen (N) cycling. In particular, loss of N due to leaching after afforestation could lead to soil C losses. However, the link between C and N changes due to afforestation has primarily been suggested by models and to my knowledge has never been explicitly tested across a precipitation gradient. The goal of this study was to test how precipitation affects changes in labile and bulk pools of soil C and N across a precipitation gradient, which will provide novel insight into the linkage between land-use change, different pools of soil C and N, and precipitation. I conducted this study across a gradient of precipitation in the Rio de la Plata grasslands of Argentina and Uruguay which ranged from 600mm to 1500mm of precipitation per year. The sites were all former grasslands that had been planted with Eucalyptus. I found that changes in bulk soil C and N were related to MAP with drier sites gaining and wetter sites losing C and N (R2=0.59, p=0.003), which supports the idea that N losses are strongly linked to C losses with afforestation. C and N in microbial biomass and extractable pools followed similar patterns to bulk soil C and N. Interestingly, losses of C and N decreased as the plantations aged, suggesting that longer rotation times for plantations could reduce potential soil carbon and nitrogen losses. These results indicate that afforestation is still be a valuable tool for carbon sequestration, but calculations of the benefits of afforestation must take into account site factors such as age and precipitation to accurately calculate total sequestration benefit and ensure continued high productivity and carbon sequestration.

In conclusion, afforestation could be an effective tool for carbon sequestration. However, its benefits need to be carefully weighed against its costs for soil such as reduced microbial diversity, decreased soil microbial functional capacity, losses of soil organic matter, and nutrient depletion. Careful management and consideration of afforestation is needed to ensure the greatest benefits with the least long-term damage to soils.