Patterns and controls of foliar nutrient stoichiometry and flexibility across United States forests.

Plant element stoichiometry and stoichiometric flexibility strongly regulate ecosystem responses to global change. Here, we tested three potential mechanistic drivers (climate, soil nutrients, and plant taxonomy) of both using paired foliar and soil nutrient data from terrestrial forested National Ecological Observatory Network sites across the USA. We found that broad patterns of foliar nitrogen (N) and foliar phosphorus (P) are explained by different mechanisms. Plant taxonomy was an important control over all foliar nutrient stoichiometries and concentrations, especially foliar N, which was dominantly related to taxonomy and did not vary across climate or soil gradients. Despite a lack of site-level correlations between N and environment variables, foliar N exhibited intraspecific flexibility, with numerous species-specific correlations between foliar N and various environmental factors, demonstrating the variable spatial and temporal scales on which foliar chemistry and stoichiometric flexibility can manifest. In addition to plant taxonomy, foliar P and N:P ratios were also linked to soil nutrient status (extractable P) and climate, especially actual evapotranspiration rates. Our findings highlight the myriad factors that influence foliar chemistry and show that broad patterns cannot be explained by a single consistent mechanism. Furthermore, differing controls over foliar N versus P suggests that each may be sensitive to global change drivers on distinct spatial and temporal scales, potentially resulting in altered ecosystem N:P ratios that have implications for processes ranging from productivity to carbon sequestration.

Phosphorus limitation of early growth differs between nitrogen-fixing and nonfixing dry tropical forest tree species.

Tropical forests are often characterized by low soil phosphorus (P) availability, suggesting that P limits plant performance. However, how seedlings from different functional types respond to soil P availability is poorly known but important for understanding and modeling forest dynamics under changing environmental conditions. We grew four nitrogen (N)-fixing Fabaceae and seven diverse non-N-fixing tropical dry forest tree species in a shade house under three P fertilization treatments and evaluated carbon (C) allocation responses, P demand, P-use, investment in P acquisition traits, and correlations among P acquisition traits. Nitrogen fixers grew larger with increasing P addition in contrast to non-N fixers, which showed fewer responses in C allocation and P use. Foliar P increased with P addition for both functional types, while P acquisition strategies did not vary among treatments but differed between functional types, with N fixers showing higher root phosphatase activity (RPA) than nonfixers. Growth responses suggest that N fixers are limited by P, but nonfixers may be limited by other resources. However, regardless of limitation, P acquisition traits such as mycorrhizal colonization and RPA were nonplastic across a steep P gradient. Differential limitation among plant functional types has implications for forest succession and earth system models.

Tracing plant-environment interactions from organismal to planetary scales using stable isotopes: a mini review.

Natural isotope variation forms a mosaic of isotopically distinct pools across the biosphere and flows between pools integrate plant ecology with global biogeochemical cycling. Carbon, nitrogen, and water isotopic ratios (among others) can be measured in plant tissues, at root and foliar interfaces, and in adjacent atmospheric, water, and soil environments. Natural abundance isotopes provide ecological insight to complement and enhance biogeochemical research, such as understanding the physiological conditions during photosynthetic assimilation (e.g. water stress) or the contribution of unusual plant water or nutrient sources (e.g. fog, foliar deposition). While foundational concepts and methods have endured through four decades of research, technological improvements that enable measurement at fine spatiotemporal scales, of multiple isotopes, and of isotopomers, are advancing the field of stable isotope ecology. For example, isotope studies now benefit from the maturation of field-portable infrared spectroscopy, which allows the exploration of plant-environment sensitivity at physiological timescales. Isotope ecology is also benefiting from, and contributing to, new understanding of the plant-soil-atmosphere system, such as improving the representation of soil carbon pools and turnover in land surface models. At larger Earth-system scales, a maturing global coverage of isotope data and new data from site networks offer exciting synthesis opportunities to merge the insights of single-or multi-isotope analysis with ecosystem and remote sensing data in a data-driven modeling framework, to create geospatial isotope products essential for studies of global environmental change.

Non-native mangroves support carbon storage, sediment carbon burial, and accretion of coastal ecosystems.

Mangrove forests play an important role in climate change adaptation and mitigation by maintaining coastline elevations relative to sea level rise, protecting coastal infrastructure from storm damage, and storing substantial quantities of carbon (C) in live and detrital pools. Determining the efficacy of mangroves in achieving climate goals can be complicated by difficulty in quantifying C inputs (i.e., differentiating newer inputs from younger trees from older residual C pools), and mitigation assessments rarely consider potential offsets to CO2 storage by methane (CH4 ) production in mangrove sediments. The establishment of non-native Rhizophora mangle along Hawaiian coastlines over the last century offers an opportunity to examine the role mangroves play in climate mitigation and adaptation both globally and locally as novel ecosystems. We quantified total ecosystem C storage, sedimentation, accretion, sediment organic C burial and CH4 emissions from ~70 year old R. mangle stands and adjacent uninvaded mudflats. Ecosystem C stocks of mangrove stands exceeded mudflats by 434 ± 33 Mg C/ha, and mangrove establishment increased average coastal accretion by 460%. Sediment organic C burial increased 10-fold (to 4.5 Mg C ha-1  year-1 ), double the global mean for old growth mangrove forests, suggesting that C accumulation from younger trees may occur faster than previously thought, with implications for mangrove restoration. Simulations indicate that increased CH4 emissions from sediments offset ecosystem CO2 storage by only 2%-4%, equivalent to 30-60 Mg CO2 -eq/ha over mangrove lifetime (100 year sustained global warming potential). Results highlight the importance of mangroves as novel systems that can rapidly accumulate C, have a net positive atmospheric greenhouse gas removal effect, and support shoreline accretion rates that outpace current sea level rise. Sequestration potential of novel mangrove forests should be taken into account when considering their removal or management, especially in the context of climate mitigation goals.

Leaf-cutter ants engineer large nitrous oxide hot spots in tropical forests.

Though tropical forest ecosystems are among the largest natural sources of the potent greenhouse gas nitrous oxide (N2O), the spatial distribution of emissions across landscapes is often poorly resolved. Leaf cutter ants (LCA; Atta and Acromyrmex, Myrmicinae) are dominant herbivores throughout Central and South America, and influence multiple aspects of forest structure and function. In particular, their foraging creates spatial heterogeneity by concentrating large quantities of organic matter (including nitrogen, N) from the surrounding canopy into their colonies, and ultimately into colony refuse dumps. Here, we demonstrate that refuse piles created by LCA species Atta colombica in tropical rainforests of Costa Rica provide ideal conditions for extremely high rates of N2O production (high microbial biomass, potential denitrification enzyme activity, N content and anoxia) and may represent an unappreciated source of heterogeneity in tropical forest N2O emissions. Average instantaneous refuse pile N2O fluxes surpassed background emissions by more than three orders of magnitude (in some cases exceeding 80 000 µg N2O-N m-2 h-1) and generating fluxes comparable to or greater than those produced by engineered systems such as wastewater treatment tanks. Refuse-concentrating Atta species are ubiquitous in tropical forests, pastures and production ecosystems, and increase density strongly in response to disturbance. As such, LCA colonies may represent an unrecognized greenhouse gas point source throughout the Neotropics.

Biogeochemical recuperation of lowland tropical forest during succession.

High rates of land conversion and land use change have vastly increased the proportion of secondary forest in the lowland tropics relative to mature forest. As secondary forests recover following abandonment, nitrogen (N) and phosphorus (P) must be present in sufficient quantities to sustain high rates of net primary production and to replenish the nutrients lost during land use prior to secondary forest establishment. Biogeochemical theory and results from individual studies suggest that N can recuperate during secondary forest recovery, especially relative to P. Here, we synthesized 23 metrics of N and P in soil and plants from 45 secondary forest chronosequences located in the wet tropics to empirically explore (1) whether there is a consistent change in nutrients and nutrient cycling processes during secondary succession in the biome; (2) which metrics of N and P in soil and plants recuperate most consistently; (3) if the recuperation of nutrients during succession approaches similar nutrient concentrations and fluxes as those in mature forest in ~100 yr following the initiation of succession; and (4) whether site characteristics, including disturbance history, climate, and soil order are significantly related to nutrient recuperation. During secondary forest succession, nine metrics of N and/or P cycling changed consistently and substantially. In most sites, N concentrations and fluxes in both plants and soil increased during secondary succession, and total P concentrations increased in surface soil. Changes in nutrient concentrations and nutrient cycling processes during secondary succession were similar whether mature forest was included or excluded from the analysis, indicating that nutrient recuperation in secondary forest leads to biogeochemical conditions that are similar to those of mature forest. Further, of the N and P metrics that recuperated, only soil total P and foliar δ15 N were strongly influenced by site characteristics like climate, soils, or disturbance history. Predictable nutrient recuperation across a diverse and productive ecosystem may support future forest growth and could provide a means to quantify successful restoration of ecosystem function in secondary tropical forest beyond biomass or species composition.

Remotely sensed canopy nitrogen correlates with nitrous oxide emissions in a lowland tropical rainforest.

Tropical forests exhibit significant heterogeneity in plant functional and chemical traits that may contribute to spatial patterns of key soil biogeochemical processes, such as carbon storage and greenhouse gas emissions. Although tropical forests are the largest ecosystem source of nitrous oxide (N2 O), drivers of spatial patterns within forests are poorly resolved. Here, we show that local variation in canopy foliar N, mapped by remote-sensing image spectroscopy, correlates with patterns of soil N2 O emission from a lowland tropical rainforest. We identified ten 0.25 ha plots (assemblages of 40-70 individual trees) in which average remotely-sensed canopy N fell above or below the regional mean. The plots were located on a single minimally-dissected terrace (<1 km2 ) where soil type, vegetation structure and climatic conditions were relatively constant. We measured N2 O fluxes monthly for 1 yr and found that high canopy N species assemblages had on average three-fold higher total mean N2 O fluxes than nearby lower canopy N areas. These differences are consistent with strong differences in litter stoichiometry, nitrification rates and soil nitrate concentrations. Canopy N status was also associated with microbial community characteristics: lower canopy N plots had two-fold greater soil fungal to bacterial ratios and a significantly lower abundance of ammonia-oxidizing archaea, although genes associated with denitrification (nirS, nirK, nosZ) showed no relationship with N2 O flux. Overall, landscape emissions from this ecosystem are at the lowest end of the spectrum reported for tropical forests, consist with multiple metrics indicating that these highly productive forests retain N tightly and have low plant-available losses. These data point to connections between canopy and soil processes that have largely been overlooked as a driver of denitrification. Defining relationships between remotely-sensed plant traits and soil processes offers the chance to map these processes at large scales, potentially increasing our ability to predict N2 O emissions in heterogeneous landscapes.

Natural abundance (δ¹5N) indicates shifts in nitrogen relations of woody taxa along a savanna-woodland continental rainfall gradient.

Water and nitrogen (N) interact to influence soil N cycling and plant N acquisition. We studied indices of soil N availability and acquisition by woody plant taxa with distinct nutritional specialisations along a north Australian rainfall gradient from monsoonal savanna (1,600-1,300 mm annual rainfall) to semi-arid woodland (600-250 mm). Aridity resulted in increased 'openness' of N cycling, indicated by increasing δ(15)N(soil) and nitrate:ammonium ratios, as plant communities transitioned from N to water limitation. In this context, we tested the hypothesis that δ(15)N(root) xylem sap provides a more direct measure of plant N acquisition than δ(15)N(foliage). We found highly variable offsets between δ(15)N(foliage) and δ(15)N(root) xylem sap, both between taxa at a single site (1.3-3.4 ‰) and within taxa across sites (0.8-3.4 ‰). As a result, δ(15)N(foliage) overlapped between N-fixing Acacia and non-fixing Eucalyptus/Corymbia and could not be used to reliably identify biological N fixation (BNF). However, Acacia δ(15)N(root) xylem sap indicated a decline in BNF with aridity corroborated by absence of root nodules and increasing xylem sap nitrate concentrations and consistent with shifting resource limitation. Acacia dominance at arid sites may be attributed to flexibility in N acquisition rather than BNF capacity. δ(15)N(root) xylem sap showed no evidence of shifting N acquisition in non-mycorrhizal Hakea/Grevillea and indicated only minor shifts in Eucalyptus/Corymbia consistent with enrichment of δ(15)N(soil) and/or decreasing mycorrhizal colonisation with aridity. We propose that δ(15)N(root) xylem sap is a more direct indicator of N source than δ(15)N(foliage), with calibration required before it could be applied to quantify BNF.

Investigating patterns of symbiotic nitrogen fixation during vegetation change from grassland to woodland using fine scale δ(15) N measurements.

Biological nitrogen fixation (BNF) in woody plants is often investigated using foliar measurements of δ(15) N and is of particular interest in ecosystems experiencing increases in BNF due to woody plant encroachment. We sampled δ(15) N along the entire N uptake pathway including soil solution, xylem sap and foliage to (1) test assumptions inherent to the use of foliar δ(15) N as a proxy for BNF; (2) determine whether seasonal divergences occur between δ(15) Nxylem sap and δ(15) Nsoil inorganic N that could be used to infer variation in BNF; and (3) assess patterns of δ(15) N with tree age as indicators of shifting BNF or N cycling. Measurements of woody N-fixing Prosopis glandulosa and paired reference non-fixing Zanthoxylum fagara at three seasonal time points showed that δ(15) Nsoil inorganic N varied temporally and spatially between species. Fractionation between xylem and foliar δ(15) N was consistently opposite in direction between species and varied on average by 2.4‰. Accounting for these sources of variation caused percent nitrogen derived from fixation values for Prosopis to vary by up to ∼70%. Soil-xylem δ(15) N separation varied temporally and increased with Prosopis age, suggesting seasonal variation in N cycling and BNF and potential long-term increases in BNF not apparent through foliar sampling alone.

Arabidopsis and Lobelia anceps access small peptides as a nitrogen source for growth.

While importance of amino acids as a nitrogen source for plants is increasingly recognised, other organic N sources including small peptides have received less attention. We assessed the capacity of functionally different species, annual and nonmycorrhizal Arabidopsis thaliana (L.) Heynh. (Brassicaceae) and perennial Lobelia anceps L.f. (Campanulaceae), to acquire, metabolise and use small peptides as a N source independent of symbionts. Plants were grown axenically on media supplemented with small peptides (2-4 amino acids), amino acids or inorganic N. In A. thaliana, peptides of up to four amino acid residues sustained growth and supported up to 74% of the maximum biomass accumulation achieved with inorganic N. Peptides also supported growth of L. anceps, but to a lesser extent. Using metabolite analysis, a proportion of the peptides supplied in the medium were detected intact in root and shoot tissue together with their metabolic products. Nitrogen source preferences, growth responses and shoot-root biomass allocation were species-specific and suggest caution in the use of Arabidopsis as the sole plant model. In particular, glycine peptides of increasing length induced effects ranging from complete inhibition to marked stimulation of root growth. This study contributes to emerging evidence that plants can acquire and metabolise organic N beyond amino acids.