Remotely detected aboveground plant function predicts belowground processes in two prairie diversity experiments.

Imaging spectroscopy provides the opportunity to incorporate leaf and canopy optical data into ecological studies, but the extent to which remote sensing of vegetation can enhance the study of belowground processes is not well understood. In terrestrial systems, aboveground and belowground vegetation quantity and quality are coupled, and both influence belowground microbial processes and nutrient cycling. We hypothesized that ecosystem productivity, and the chemical, structural and phylogenetic-functional composition of plant communities would be detectable with remote sensing and could be used to predict belowground plant and soil processes in two grassland biodiversity experiments: the BioDIV experiment at Cedar Creek Ecosystem Science Reserve in Minnesota and the Wood River Nature Conservancy experiment in Nebraska. We tested whether aboveground vegetation chemistry and productivity, as detected from airborne sensors, predict soil properties, microbial processes and community composition. Imaging spectroscopy data were used to map aboveground biomass, green vegetation cover, functional traits and phylogenetic-functional community composition of vegetation. We examined the relationships between the image-derived variables and soil carbon and nitrogen concentration, microbial community composition, biomass and extracellular enzyme activity, and soil processes, including net nitrogen mineralization. In the BioDIV experiment-which has low overall diversity and productivity despite high variation in each-belowground processes were driven mainly by variation in the amount of organic matter inputs to soils. As a consequence, soil respiration, microbial biomass and enzyme activity, and fungal and bacterial composition and diversity were significantly predicted by remotely sensed vegetation cover and biomass. In contrast, at Wood River-where plant diversity and productivity were consistently higher-belowground processes were driven mainly by variation in the quality of aboveground inputs to soils. Consequently, remotely sensed functional, chemical and phylogenetic composition of vegetation predicted belowground extracellular enzyme activity, microbial biomass, and net nitrogen mineralization rates but aboveground biomass (or cover) did not. The contrasting associations between the quantity (productivity) and quality (composition) of aboveground inputs with belowground soil attributes provide a basis for using imaging spectroscopy to understand belowground processes across productivity gradients in grassland systems. However, a mechanistic understanding of how above and belowground components interact among different ecosystems remains critical to extending these results broadly.

Coupling spectral and resource-use complementarity in experimental grassland and forest communities.

Reflectance spectra provide integrative measures of plant phenotypes by capturing chemical, morphological, anatomical and architectural trait information. Here, we investigate the linkages between plant spectral variation, and spectral and resource-use complementarity that contribute to ecosystem productivity. In both a forest and prairie grassland diversity experiment, we delineated n-dimensional hypervolumes using wavelength bands of reflectance spectra to test the association between the spectral space occupied by individual plants and their growth, as well as between the spectral space occupied by plant communities and ecosystem productivity. We show that the spectral space occupied by individuals increased with their growth, and the spectral space occupied by plant communities increased with ecosystem productivity. Furthermore, ecosystem productivity was better explained by inter-individual spectral complementarity than by the large spectral space occupied by productive individuals. Our results indicate that spectral hypervolumes of plants can reflect ecological strategies that shape community composition and ecosystem function, and that spectral complementarity can reveal resource-use complementarity.

Plant spectral diversity integrates functional and phylogenetic components of biodiversity and predicts ecosystem function.

Biodiversity promotes ecosystem function as a consequence of functional differences among organisms that enable resource partitioning and facilitation. As the need for biodiversity assessments increases in the face of accelerated global change, novel approaches that are rapid, repeatable and scalable are critical, especially in ecosystems for which information about species identity and the number of species is difficult to acquire. Here, we present 'spectral diversity'-a spectroscopic index of the variability of electromagnetic radiation reflected from plants measured in the visible, near-infrared and short-wave infrared regions (400-2,400 nm). Using data collected from the Cedar Creek biodiversity experiment (Minnesota, USA), we provide evidence that the dissimilarity of species' leaf spectra increases with functional dissimilarity and evolutionary divergence time. Spectral diversity at the leaf level explains 51% of total variation in productivity-a proportion comparable to taxonomic (47%), functional (51%) or phylogenetic diversity (48%)-and performs similarly when calculated from high-resolution canopy image spectra. Spectral diversity is an emerging dimension of plant biodiversity that integrates trait variation within and across species even in the absence of taxonomic, functional, phylogenetic or abundance information, and has the potential to transform biodiversity assessment because of its scalability to remote sensing.

Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem.

It is commonly assumed that microbial communities are structured by "bottom-up" ecological forces, although few experimental manipulations have rigorously tested the mechanisms by which resources structure soil communities. We investigated how plant substrate availability might structure fungal communities and belowground processes along an experimental plant richness gradient in a grassland ecosystem. We hypothesized that variation in total plant-derived substrate inputs, plant functional group diversity, as well as the relative abundance of C4 grasses and legumes would modulate fungal α- and ß-diversity and their rates of soil carbon (C) and nitrogen (N) cycling. To test these predictions, we molecularly characterized fungal communities, as well as potential extracellular enzyme activity, net N mineralization, and soil organic matter respiration. We found higher fungal richness was associated with increasing aboveground plant biomass; whereas, fungal ß-diversity was explained by contributions from C4 grass and legume relative dominance, plant functional group diversity, as well as plant biomass. Furthermore, aboveground plant biomass consistently shaped the richness and composition of individual fungal trophic modes (i.e., saprotrophs, symbiotrophs, pathotrophs). Finally, variation in extracellular enzyme activity, net N mineralization rates, and soil organic matter respiration was significantly explained by fungal ß-diversity when fungi were functionally classified. Via changes in the supply and composition of organic substrates entering soil, our study demonstrates that changes in the plant species richness and functional composition collectively influence fungal communities and rates of soil C and N cycling.

Condensed tannins increase nitrogen recovery by trees following insect defoliation.

While the importance of plant secondary metabolites to belowground functioning is gaining recognition, the perception remains that secondary metabolites are produced for herbivore defense, whereas their belowground impacts are ecological by-products, or 'afterlife' effects. However, plants invest a significant amount of resources into production of secondary metabolites that have minimal effects on herbivore resistance (e.g. condensed tannins and insect herbivores). We show that genetically mediated variation in condensed tannin concentration is correlated with plant nitrogen recovery following a severe defoliation event. We used single-tree mesocosms labeled with (15) N to track nitrogen through both the frass and litter cycling pathways. High concentrations of leaf tannins in Populus tremuloides were correlated with (15) N recovery from frass within the same growing season and in the following growing season. Likewise, leaf tannin concentrations were also correlated with (15) N recovery from the litter of defoliated trees in the growing season following the defoliation event. Conversely, tannins were not well correlated with nitrogen uptake under conditions of nominal herbivory. Our results suggest that tannins may confer benefits in response to herbivore pressure through conserved belowground nitrogen cycling, rather than via defensive properties. Consequently, tannins may be considered as chemical mediators of tolerance rather than resistance.

Imaging spectroscopy links aspen genotype with below-ground processes at landscape scales.

Fine-scale biodiversity is increasingly recognized as important to ecosystem-level processes. Remote sensing technologies have great potential to estimate both biodiversity and ecosystem function over large spatial scales. Here, we demonstrate the capacity of imaging spectroscopy to discriminate among genotypes of Populus tremuloides (trembling aspen), one of the most genetically diverse and widespread forest species in North America. We combine imaging spectroscopy (AVIRIS) data with genetic, phytochemical, microbial and biogeochemical data to determine how intraspecific plant genetic variation influences below-ground processes at landscape scales. We demonstrate that both canopy chemistry and below-ground processes vary over large spatial scales (continental) according to aspen genotype. Imaging spectrometer data distinguish aspen genotypes through variation in canopy spectral signature. In addition, foliar spectral variation correlates well with variation in canopy chemistry, especially condensed tannins. Variation in aspen canopy chemistry, in turn, is correlated with variation in below-ground processes. Variation in spectra also correlates well with variation in soil traits. These findings indicate that forest tree species can create spatial mosaics of ecosystem functioning across large spatial scales and that these patterns can be quantified via remote sensing techniques. Moreover, they demonstrate the utility of using optical properties as proxies for fine-scale measurements of biodiversity over large spatial scales.

Widespread triploidy in Western North American aspen (Populus tremuloides).

We document high rates of triploidy in aspen (Populus tremuloides) across the western USA (up to 69% of genets), and ask whether the incidence of triploidy across the species range corresponds with latitude, glacial history (as has been documented in other species), climate, or regional variance in clone size. Using a combination of microsatellite genotyping, flow cytometry, and cytology, we demonstrate that triploidy is highest in unglaciated, drought-prone regions of North America, where the largest clone sizes have been reported for this species. While we cannot completely rule out a low incidence of undetected aneuploidy, tetraploidy or duplicated loci, our evidence suggests that these phenomena are unlikely to be significant contributors to our observed patterns. We suggest that the distribution of triploid aspen is due to a positive synergy between triploidy and ecological factors driving clonality. Although triploids are expected to have low fertility, they are hypothesized to be an evolutionary link to sexual tetraploidy. Thus, interactions between clonality and polyploidy may be a broadly important component of geographic speciation patterns in perennial plants. Further, cytotypes are expected to show physiological and structural differences which may influence susceptibility to ecological factors such as drought, and we suggest that cytotype may be a significant and previously overlooked factor in recent patterns of high aspen mortality in the southwestern portion of the species range. Finally, triploidy should be carefully considered as a source of variance in genomic and ecological studies of aspen, particularly in western U.S. landscapes.

From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization.

Using two genetic approaches and seven different plant systems, we present findings from a meta-analysis examining the strength of the effects of plant genetic introgression and genotypic diversity across individual, community and ecosystem levels with the goal of synthesizing the patterns to date. We found that (i) the strength of plant genetic effects can be quite high; however, the overall strength of genetic effects on most response variables declined as the levels of organization increased. (ii) Plant genetic effects varied such that introgression had a greater impact on individual phenotypes than extended effects on arthropods or microbes/fungi. By contrast, the greatest effects of genotypic diversity were on arthropods. (iii) Plant genetic effects were greater on above-ground versus below-ground processes, but there was no difference between terrestrial and aquatic environments. (iv) The strength of the effects of intraspecific genotypic diversity tended to be weaker than interspecific genetic introgression. (v) Although genetic effects generally decline across levels of organization, in some cases they do not, suggesting that specific organisms and/or processes may respond more than others to underlying genetic variation. Because patterns in the overall impacts of introgression and genotypic diversity were generally consistent across diverse study systems and consistent with theoretical expectations, these results provide generality for understanding the extended consequences of plant genetic variation across levels of organization, with evolutionary implications.

Genetic mosaics of ecosystem functioning across aspen-dominated landscapes.

Genetic diversity is the foundation of all biodiversity, and the genetic variation within species is increasingly recognized as being important to ecosystem level processes. Recent research demonstrates that plant genotype influences above- and belowground communities as well as basic ecosystem functions. However, the extent to which plant genotypes create spatial mosaics of genetically mediated ecosystem processes in natural forests is uncertain. We use Populus tremuloides as a model system to demonstrate the importance of plant genotype on carbon and nitrogen cycling in natural systems. We identified 24 distinct P. tremuloides clones with multiple ramets across 25 km(2) in southern Wisconsin, United States, using microsatellite makers. We then sampled clone leaf chemistry and belowground nutrient content and microbial extracellular enzyme activity. Aspen-induced variation in belowground carbon and nitrogen content, and microbial activity, varied widely among clones. Variation in green leaf chemistry and belowground microbial activity were correlated with genetic distance among clones, such that more genetically distant clones created more divergent patches of ecosystem processes. These data suggest that aspen genotypes create spatial mosaics of genetically mediated ecosystem functioning across natural landscapes and can therefore have evolutionary consequences for co-occurring species.

Intraspecific litter diversity and nitrogen deposition affect nutrient dynamics and soil respiration.

Anthropogenic forces are concurrently reducing biodiversity and altering terrestrial nutrient cycles. As natural populations decline, genetic diversity within single species also declines. The consequences of intraspecific genetic loss for ecosystem functions are poorly understood, and interactions among intraspecific diversity, nitrogen deposition, and nutrient cycling are unknown. We present results from an experiment that simulated both a decline in biodiversity and an increase in nitrogen deposition. In soil microcosms, we tested effects of variation in intraspecific litter diversity and nitrogen deposition on soil respiration and nitrogen leaching. Increases in intraspecific litter diversity increased soil respiration overall, with the greatest increases in respiration occurring under high nitrogen deposition. Nitrogen deposition increased the amount of inorganic nitrogen leached, while the amount of dissolved organic nitrogen leached was correlated with initial litter chemistry (lignin concentration) and remained independent of litter diversity and nitrogen deposition treatments. Our results demonstrate the potential for losses in genetic diversity to interact with other global environmental changes to influence terrestrial nutrient cycles.