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- Plant Physiology
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- National Science Foundation
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BACKGROUND The availability of nitrogen (N) to plants and microbes has a major influence on the structure and function of ecosystems. Because N is an essential component of plant proteins, low N availability constrains the growth of plants and herbivores. To increase N availability, humans apply large amounts of fertilizer to agricultural systems. Losses from these systems, combined with atmospheric deposition of fossil fuel combustion products, introduce copious quantities of reactive N into ecosystems. The negative consequences of these anthropogenic N inputs—such as ecosystem eutrophication and reductions in terrestrial and aquatic biodiversity—are well documented. Yet although N availability is increasing in many locations, reactive N inputs are not evenly distributed globally. Furthermore, experiments and theory also suggest that global change factors such as elevated atmospheric CO 2 , rising temperatures, and altered precipitation and disturbance regimes can reduce the availability of N to plants and microbes in many terrestrial ecosystems. This can occur through increases in biotic demand for N or reductions in its supply to organisms. Reductions in N availability can be observed via several metrics, including lowered nitrogen concentrations ([N]) and isotope ratios (δ 15 N) in plant tissue, reduced rates of N mineralization, and reduced terrestrial N export to aquatic systems. However, a comprehensive synthesis of N availability metrics, outside of experimental settings and capable of revealing large-scale trends, has not yet been carried out. ADVANCES A growing body of observations confirms that N availability is declining in many nonagricultural ecosystems worldwide. Studies have demonstrated declining wood δ 15 N in forests across the continental US, declining foliar [N] in European forests, declining foliar [N] and δ 15 N in North American grasslands, and declining [N] in pollen from the US and southern Canada. This evidence is consistent with observed global-scale declines in foliar δ 15 N and [N] since 1980. Long-term monitoring of soil-based N availability indicators in unmanipulated systems is rare. However, forest studies in the northeast US have demonstrated decades-long decreases in soil N cycling and N exports to air and water, even in the face of elevated atmospheric N deposition. Collectively, these studies suggest a sustained decline in N availability across a range of terrestrial ecosystems, dating at least as far back as the early 20th century. Elevated atmospheric CO 2 levels are likely a main driver of declines in N availability. Terrestrial plants are now uniformly exposed to ~50% more of this essential resource than they were just 150 years ago, and experimentally exposing plants to elevated CO 2 often reduces foliar [N] as well as plant-available soil N. In addition, globally-rising temperatures may raise soil N supply in some systems but may also increase N losses and lead to lower foliar [N]. Changes in other ecosystem drivers—such as local climate patterns, N deposition rates, and disturbance regimes—individually affect smaller areas but may have important cumulative effects on global N availability. OUTLOOK Given the importance of N to ecosystem functioning, a decline in available N is likely to have far-reaching consequences. Reduced N availability likely constrains the response of plants to elevated CO 2 and the ability of ecosystems to sequester carbon. Because herbivore growth and reproduction scale with protein intake, declining foliar [N] may be contributing to widely reported declines in insect populations and may be negatively affecting the growth of grazing livestock and herbivorous wild mammals. Spatial and temporal patterns in N availability are not yet fully understood, particularly outside of Europe and North America. Developments in remote sensing, accompanied by additional historical reconstructions of N availability from tree rings, herbarium specimens, and sediments, will show how N availability trajectories vary among ecosystems. Such assessment and monitoring efforts need to be complemented by further experimental and theoretical investigations into the causes of declining N availability, its implications for global carbon sequestration, and how its effects propagate through food webs. Responses will need to involve reducing N demand via lowering atmospheric CO 2 concentrations, and/or increasing N supply. Successfully mitigating and adapting to declining N availability will require a broader understanding that this phenomenon is occurring alongside the more widely recognized issue of anthropogenic eutrophication. Intercalibration of isotopic records from leaves, tree rings, and lake sediments suggests that N availability in many terrestrial ecosystems has steadily declined since the beginning of the industrial era. Reductions in N availability may affect many aspects of ecosystem functioning, including carbon sequestration and herbivore nutrition. Shaded areas indicate 80% prediction intervals; marker size is proportional to the number of measurements in each annual mean. Isotope data: (tree ring) K. K. McLauchlan et al. , Sci. Rep. 7 , 7856 (2017); (lake sediment) G. W. Holtgrieve et al. , Science 334 , 1545–1548 (2011); (foliar) J. M. Craine et al. , Nat. Ecol. Evol. 2 , 1735–1744 (2018)more » « less
Climate models for the northeastern United States (U.S.) over the next century predict an increase in air temperature between 2.8 and 4.3 °C and a decrease in the average number of days per year when a snowpack will cover the forest floor (Hayhoe et al. 2007, 2008; Campbell et al. 2010). Studies of forest dynamics in seasonally snow-covered ecosystems have been primarily conducted during the growing season, when most biological activity occurs. However, in recent years considerable progress has been made in our understanding of how winter climate change influences dynamics in these forests. The snowpack insulates soil from below-freezing air temperatures, which facilitates a significant amount of microbial activity. However, a smaller snowpack and increased depth and duration of soil frost amplify losses of dissolved organic C and NO3- in leachate, as well as N2O released into the atmosphere. The increase in nutrient loss following increased soil frost cannot be explained by changes in microbial activity alone. More likely, it is caused by a decrease in plant nutrient uptake following increases in soil frost. We conducted a snow-removal experiment at Hubbard Brook Experimental Forest to determine the effects of a smaller winter snowpack and greater depth and duration of soil frost on trees, soil microbes, and arthropods. A number of publications have been based on these data: Comerford et al. 2013, Reinmann et al. 2019, Templer 2012, and Templer et al. 2012. These data were gathered as part of the Hubbard Brook Ecosystem Study (HBES). The HBES is a collaborative effort at the Hubbard Brook Experimental Forest, which is operated and maintained by the USDA Forest Service, Northern Research Station. Campbell JL, Ollinger SV, Flerchinger GN, Wicklein H, Hayhoe K, Bailey AS. Past and projected future changes in snowpack and soil frost at the Hubbard Brook Experimental Forest, New Hampshire, USA. Hydrological Processes. 2010; 24:2465–2480. Comerford DP, PG Schaberg, PH Templer, AM Socci, JL Campbell, and KF Wallin. 2013. Influence of experimental snow removal on root and canopy physiology of sugar maple trees in a northern hardwood forest. Oecologia 171:261-269. Hayhoe K, Wake CP, Huntington TG, Luo LF, Schwartz MD, Sheffield J, et al. Past and future changes in climate and hydrological indicators in the US Northeast. Climate Dynamics. 2007; 28:381–407. Hayhoe, K., Wake, C., Anderson, B. et al. Regional climate change projections for the Northeast USA. Mitig Adapt Strateg Glob Change 13, 425–436 (2008). https://doi.org/10.1007/s11027-007-9133-2. Reinmann AB, J Susser, EMC Demaria, PH Templer. 2019. Declines in northern forest tree growth following snowpack decline and soil freezing. Global Change Biology 25:420-430. Templer PH. 2012. Changes in winter climate: soil frost, root injury, and fungal communities (Invited). Plant and Soil 35: 15-17 Templer PH , AF Schiller, NW Fuller, AM Socci, JL Campbell, JE Drake, and TH Kunz. 2012. Impact of a reduced winter snowpack on litter arthropod abundance and diversity in a northern hardwood forest ecosystem. Biology and Fertility of Soils 48:413-424.more » « less
null (Ed.)Terrestrial ecosystems are increasingly enriched with resources such as atmospheric CO 2 that limit ecosystem processes. The consequences for ecosystem carbon cycling depend on the feedbacks from other limiting resources and plant community change, which remain poorly understood for soil CO 2 efflux, J CO2 , a primary carbon flux from the biosphere to the atmosphere. We applied a unique CO 2 enrichment gradient (250 to 500 µL L −1 ) for eight years to grassland plant communities on soils from different landscape positions. We identified the trajectory of J CO2 responses and feedbacks from other resources, plant diversity [effective species richness, exp(H)], and community change (plant species turnover). We found linear increases in J CO2 on an alluvial sandy loam and a lowland clay soil, and an asymptotic increase on an upland silty clay soil. Structural equation modeling identified CO 2 as the dominant limitation on J CO2 on the clay soil. In contrast with theory predicting limitation from a single limiting factor, the linear J CO2 response on the sandy loam was reinforced by positive feedbacks from aboveground net primary productivity and exp(H), while the asymptotic J CO2 response on the silty clay arose from a net negative feedback among exp(H), species turnover, and soil water potential. These findings support a multiple resource limitation view of the effects of global change drivers on grassland ecosystem carbon cycling and highlight a crucial role for positive or negative feedbacks between limiting resources and plant community structure. Incorporating these feedbacks will improve models of terrestrial carbon sequestration and ecosystem services.more » « less
Chi Fru, Ernest ; Chik, Alex ; Colwell, Fredrick ; Dittrich, Maria ; Engel, Annette ; Keenan, Sarah ; Meckenstock, Rainer ; Omelon, Christopher ; Purkamo, Lotta ; Weisener, Chris (Ed.)
Roots are common features in basaltic lava tube caves on the island of Hawai‘i. For the past 50 years, new species of cave-adapted invertebrates, including cixiid planthoppers, crickets, thread-legged bugs, and spiders, have been discovered from root patches in lava tubes on different volcanoes and across variable climatic conditions. Assessing vegetation on the surface above lava tube passages, as well as genetic characterization of roots from within lava tubes, suggest that most roots belong to the native pioneer tree, ‘ōhi‘a lehua (
Metrosideros polymorpha). Planthoppers are the primary consumers of sap at the base of the subsurface food web. However, root physicochemistry and rhizobiome microbial diversity and functional potential have received little attention. This study focuses on characterizing the ‘ōhi‘a rhizobiome, accessed from free-hanging roots inside lava tubes. Using these results, we can begin to evaluate the development and evolution of plant-microbe-invertebrate relationships.
We explored lava tubes formed in flows of differing elevations and ages, from about 140 to 3000 years old, on Mauna Loa, Kīlauea, and Hualālai volcanoes on Hawai‘i Island. Invertebrate diversity was evaluated from root galleries and non-root galleries, in situ fluid physicochemistry was measured, and root and bare rock fluids (e.g., water, sap) were collected to determine major ion concentrations, as well as non-purgeable organic carbon (NPOC) and total nitrogen (TN) content. To verify root identity, DNA was extracted, and three sets of primers were used. After screening for only
Metrosiderosspp., the V4 region of the 16S rRNA gene was sequenced and taxonomy was assigned.
Root fluids were viscous and ranged in color from clear to yellow to reddish orange. Root fluids had 2X to 10X higher major ion concentrations compared to rock water. The average root NPOC and TN concentrations were 192 mg/L and 5.2 mg/L, respectively, compared to rock water that had concentrations of 6.8 mg/L and 1.8 mg/L, respectively. Fluids from almost 300 root samples had pH values that ranged from 2.2 to 5.6 (average pH 4.63) and were lower than rock water (average pH 6.39). Root fluid pH was comparable to soil pH from montane wet forests dominated by ‘ōhi‘a (Selmants et al. 2016), which can grow in infertile soil with pH values as low as 3.6. On Hawai‘i, rain water pH averages 5.2 at sea level and systematically decreases with elevation to pH 4.3 at 2500 m (Miller and Yoshinaga 2012), but root fluid pH did not correlate with elevation, temperature, relative humidity, inorganic and organic constituents, or age of flow. Root fluid acidity is likely due to concentrated organic compounds, sourced as root exudates, and this habitat is acidic for the associated invertebrates.
From 62 root samples, over 66% were identified to the genus
Metrosideros. A few other identifications of roots from lava tube systems where there had been extensive clear-cutting and ranching included monkey pod tree, coconut palm, Ficusspp., and silky oak.
The 16S rRNA gene sequence surveys revealed that root bacterial communities were dominated by few groups, including Burkholderiaceae, as well as Acetobacteraceae, Sphingomonadaceae, Acidobacteriaceae, Gemmataceae, Xanthobacteraceae, and Chitinophagaceae. However, most of the reads could not be classified to a specific genus, which suggested that the rhizobiome harbor novel diversity. Diversity was higher from wetter climates. The root communities were distinct from those described previously from ‘ōhi‘a flowers and leaves (Junker and Keller 2015) and lava tube rocky surfaces (Hathaway et al. 2014) where microbial groups were specifically presumed capable of heterotrophy, methanotrophy, diazotrophy, and nitrification. Less can be inferred for the rhizobiome metabolism, although most taxa are likely aerobic heterotrophs. Within the Burkholderiaceae, there were high relative abundances of sequences affiliated with the genus
Paraburkholderia, which includes known plant symbionts, as well as the acidophilic genera Acidocellaand Acidisomafrom the Acetobacteraceae, which were retrieved predominately from caves in the oldest lava flows that also had the lowest root pH values. It is likely that the bacterial groups are capable of degrading exudates and providing nutritional substrates for invertebrate consumers that are not provided by root fluids (i.e., phloem) alone.
As details about the biochemistry of ‘ōhi‘a have been missing, characterizing the rhizobiome from lava tubes will help to better understand potential plant-microbe-invertebrate interactions and ecological and evolutionary relationships through time. In particular, the microbial rhizobiome may produce compounds used by invertebrates nutritionally or that affect their behavior, and changes to the rhizobiome in response to environmental conditions may influence invertebrate interactions with the roots, which could be important to combat climate change effects or invasive species introductions.
null (Ed.)Coastal salt marshes are distributed widely across the globe and are considered essential habitat for many fish and crustacean species. Yet, the literature on fishery support by salt marshes has largely been based on a few geographically distinct model systems, and as a result, inadequately captures the hierarchical nature of salt marsh pattern, process, and variation across space and time. A better understanding of geographic variation and drivers of commonalities and differences across salt marsh systems is essential to informing future management practices. Here, we address the key drivers of geographic variation in salt marshes: hydroperiod, seascape configuration, geomorphology, climatic region, sediment supply and riverine input, salinity, vegetation composition, and human activities. Future efforts to manage, conserve, and restore these habitats will require consideration of how environmental drivers within marshes affect the overall structure and subsequent function for fisheries species. We propose a future research agenda that provides both the consistent collection and reporting of sources of variation in small-scale studies and collaborative networks running parallel studies across large scales and geographically distinct locations to provide analogous information for data poor locations. These comparisons are needed to identify and prioritize restoration or conservation efforts, identify sources of variation among regions, and best manage fisheries and food resources across the globe. Introduction Understanding the drivers of geographic variation in the condition and composition of habitats is crucial to our capacity to generalize management plans across space and time and to clarify and perhaps challenge assumptions of functional equivalence among sites. Broadly defined wetland types such as salt marshes are often assumed to provide similar functions throughout their global range, such as providing nursery habitat for fishery species. However, a growing body of evidence suggests substantial geographic variation in the functioning of salt marsh and other coastal ecosystems (Bradley et al. 2020; Whalen et al. 2020). Variation in ecological patterns and processes within habitat types can alter community structure and dynamics. Local-scale patterns and processes (e.g., patch [10s of meters], local [100s of meters]) can be influenced by processes that occur at larger spatial scales (e.g., regional [kms], global), thereby causing geographic differences in the function and ecosystem service delivery of a given habitat type. Salt marshes (which include vegetated platform, interconnected tidal creeks, fringing mudflats, ponds, and pools) are widely distributed (Fig. 1) and function as valuable nursery habitats by providing key resources for many estuarine species that transition to marine or aquatic habitats as adults (Beck et al. 2001; Minello et al. 2003; Sheaves et al. 2015). However, factors that underlie variability in the delivery of ecological functions are still inadequately understood. Previous studies have explored geographic variation in the function of salt marshes for fish and mobile crustaceans (“nekton”; e.g., Minello et al. 2012, Baker et al. 2013). However, field studies that compare multiple sites across a geographical gradient are typically limited in duration and scale. In addition, the explanatory variables (e.g., elevation, flooding duration, plant structure) collected by smaller scale studies are often inconsistent and therefore limit generalizations across sites.more » « less