Adam Wolf

Evolutionarily Stable Strategy Carbon Allocation to Foliage, Wood, and Fine Roots in Trees Competing for Light and Nitrogen: An Analytically Tractable, Individual-Based Model and Quantitative Comparisons to Data

We present a model that scales from the physiological and structural traits of individual trees competing for light and nitrogen across a gradient of soil nitrogen to their community-level consequences. The model predicts the most competitive (i.e., the evolutionarily stable strategy [ESS]) allocations to foliage, wood, and fine roots for canopy and understory stages of trees growing in old-growth forests. The ESS allocations, revealed as analytical functions of commonly measured physiological parameters, depend not on simple root-shoot relations but rather on diminishing returns of carbon investment that ensure any alternate strategy will underperform an ESS in monoculture because of the competitive environment that the ESS creates. As such, ESS allocations do not maximize nitrogen-limited growth rates in monoculture, highlighting the underappreciated idea that the most competitive strategy is not necessarily the “best,” but rather that which creates conditions in which all others are “worse.” Data from 152 stands support the model’s surprising prediction that the dominant structural trade-off is between fine roots and wood, not foliage, suggesting the “root-shoot” trade-off is more precisely a “root-stem” trade-off for long-lived trees. Assuming other resources are abundant, the model predicts that forests are limited by both nitrogen and light, or nearly so.

Global nutrient transport in a world of giants

Significance Animals play an important role in the transport of nutrients, but this role has diminished because many of the largest animals have gone extinct or experienced massive population declines. Here, we quantify the movement of nutrients by animals in the land, sea, rivers, and air both now and prior to their widespread reductions. The capacity to move nutrients away from hotspots decreased to 6% of past values across land and ocean. The vertical movement of phosphorus (P) by marine mammals was reduced by 77% and movement of P from sea to land by seabirds and anadromous fish was reduced by 96%, effectively disrupting an efficient nutrient distribution pump that once existed from the deep sea to the continental interiors. The past was a world of giants, with abundant whales in the sea and large animals roaming the land. However, that world came to an end following massive late-Quaternary megafauna extinctions on land and widespread population reductions in great whale populations over the past few centuries. These losses are likely to have had important consequences for broad-scale nutrient cycling, because recent literature suggests that large animals disproportionately drive nutrient movement. We estimate that the capacity of animals to move nutrients away from concentration patches has decreased to about 8% of the preextinction value on land and about 5% of historic values in oceans. For phosphorus (P), a key nutrient, upward movement in the ocean by marine mammals is about 23% of its former capacity (previously about 340 million kg of P per year). Movements by seabirds and anadromous fish provide important transfer of nutrients from the sea to land, totalling ∼150 million kg of P per year globally in the past, a transfer that has declined to less than 4% of this value as a result of the decimation of seabird colonies and anadromous fish populations. We propose that in the past, marine mammals, seabirds, anadromous fish, and terrestrial animals likely formed an interlinked system recycling nutrients from the ocean depths to the continental interiors, with marine mammals moving nutrients from the deep sea to surface waters, seabirds and anadromous fish moving nutrients from the ocean to land, and large animals moving nutrients away from hotspots into the continental interior.

Simulating greenhouse gas budgets of four California cropping systems under conventional and alternative management

Despite the importance of agriculture in Californias Central Valley, the potential of alternative management practices to reduce soil greenhouse gas (GHG) emissions has been poorly studied in California. This study aims at (1) calibrating and validating DAYCENT, an ecosystem model, for conventional and alternative cropping systems in Californias Central Valley, (2) estimating CO2, N2O, and CH4 soil fluxes from these systems, and (3) quantifying the uncertainty around model predictions induced by variability in the input data. The alternative practices considered were cover cropping, organic practices, and conservation tillage. These practices were compared with conventional agricultural management. The crops considered were beans, corn, cotton, safflower, sunflower, tomato, and wheat. Four field sites, for which at least five years of measured data were available, were used to calibrate and validate the DAYCENT model. The model was able to predict 86-94% of the measured variation in crop yields and 69-87% of the measured variation in soil organic carbon (SOC) contents. A Monte Carlo analysis showed that the predicted variability of SOC contents, crop yields, and N2O fluxes was generally smaller than the measured variability of these parameters, in particular for N2O fluxes. Conservation tillage had the smallest potential to reduce GHG emissions among the alternative practices evaluated, with a significant reduction of the net soil GHG fluxes in two of the three sites of 336 +/- 47 and 550 +/- 123 kg CO2-eq x ha(-1) x yr(-1) (mean +/- SE). Cover cropping had a larger potential, with net soil GHG flux reductions of 752 +/- 10, 1072 +/- 272, and 2201 +/- 82 kg CO2-eq x ha(-1) x yr(-1). Organic practices had the greatest potential for soil GHG flux reduction, with 4577 +/- 272 kg CO2-eq x ha(-1) x yr(-1). Annual differences in weather or management conditions contributed more to the variance in annual GHG emissions than soil variability did. We concluded that the DAYCENT model was successful at predicting GHG emissions of different alternative management systems in California, but that a sound error analysis must accompany the predictions to understand the risks and potentials of GHG mitigation through adoption of alternative practices.

Lateral Diffusion of Nutrients by Mammalian Herbivores in Terrestrial Ecosystems

Animals translocate nutrients by consuming nutrients at one point and excreting them or dying at another location. Such lateral fluxes may be an important mechanism of nutrient supply in many ecosystems, but lack quantification and a systematic theoretical framework for their evaluation. This paper presents a mathematical framework for quantifying such fluxes in the context of mammalian herbivores. We develop an expression for lateral diffusion of a nutrient, where the diffusivity is a biologically determined parameter depending on the characteristics of mammals occupying the domain, including size-dependent phenomena such as day range, metabolic demand, food passage time, and population size. Three findings stand out: (a) Scaling law-derived estimates of diffusion parameters are comparable to estimates calculated from estimates of each coefficient gathered from primary literature. (b) The diffusion term due to transport of nutrients in dung is orders of magnitude large than the coefficient representing nutrients in bodymass. (c) The scaling coefficients show that large herbivores make a disproportionate contribution to lateral nutrient transfer. We apply the diffusion equation to a case study of Kruger National Park to estimate the conditions under which mammal-driven nutrient transport is comparable in magnitude to other (abiotic) nutrient fluxes (inputs and losses). Finally, a global analysis of mammalian herbivore transport is presented, using a comprehensive database of contemporary animal distributions. We show that continents vary greatly in terms of the importance of animal-driven nutrient fluxes, and also that perturbations to nutrient cycles are potentially quite large if threatened large herbivores are driven to extinction.

Optimal stomatal behavior with competition for water and risk of hydraulic impairment

Significance Plants lose water and take up carbon through stomata, whose behavior has major influences on global carbon and water fluxes. Yet both competition for water and the potential fitness costs of hydraulic damage during water stress could alter how stomata behave. Here, we add variable xylem conductivity to water and carbon costs of low-xylem water potentials to the classic stomatal optimization and a pure carbon-maximization optimization. We show that both optimizations can reproduce known stomatal responses to environmental conditions but that the pure carbon-maximization optimization is also consistent with competition for water. We describe a new measure—the marginal xylem tension efficiency—that can be used to test stomatal optimizations. For over 40 y the dominant theory of stomatal behavior has been that plants should open stomates until the carbon gained by an infinitesimal additional opening balances the additional water lost times a water price that is constant at least over short periods. This theory has persisted because of its remarkable success in explaining strongly supported simple empirical models of stomatal conductance, even though we have also known for over 40 y that the theory is not consistent with competition among plants for water. We develop an alternative theory in which plants maximize carbon gain without pricing water loss and also add two features to both this and the classical theory, which are strongly supported by empirical evidence: (i) water flow through xylem that is progressively impaired as xylem water potential drops and (ii) fitness or carbon costs associated with low water potentials caused by a variety of mechanisms, including xylem damage repair. We show that our alternative carbon-maximization optimization is consistent with plant competition because it yields an evolutionary stable strategy (ESS)—species with the ESS stomatal behavior that will outcompete all others. We further show that, like the classical theory, the alternative theory also explains the functional forms of empirical stomatal models. We derive ways to test between the alternative optimization criteria by introducing a metric—the marginal xylem tension efficiency, which quantifies the amount of photosynthesis a plant will forego from opening stomatal an infinitesimal amount more to avoid a drop in water potential.

Global patterns of drought recovery.

Drought, a recurring phenomenon with major impacts on both human and natural systems, is the most widespread climatic extreme that negatively affects the land carbon sink. Although twentieth-century trends in drought regimes are ambiguous, across many regions more frequent and severe droughts are expected in the twenty-first century. Recovery time—how long an ecosystem requires to revert to its pre-drought functional state—is a critical metric of drought impact. Yet the factors influencing drought recovery and its spatiotemporal patterns at the global scale are largely unknown. Here we analyse three independent datasets of gross primary productivity and show that, across diverse ecosystems, drought recovery times are strongly associated with climate and carbon cycle dynamics, with biodiversity and CO2 fertilization as secondary factors. Our analysis also provides two key insights into the spatiotemporal patterns of drought recovery time: first, that recovery is longest in the tropics and high northern latitudes (both vulnerable areas of Earth’s climate system) and second, that drought impacts (assessed using the area of ecosystems actively recovering and time to recovery) have increased over the twentieth century. If droughts become more frequent, as expected, the time between droughts may become shorter than drought recovery time, leading to permanently damaged ecosystems and widespread degradation of the land carbon sink.

Allometric growth and allocation in forests: a perspective from FLUXNET

To develop a scheme for partitioning the products of photosynthesis toward different biomass components in land-surface models, a database on component mass and net primary productivity (NPP), collected from FLUXNET sites, was examined to determine allometric patterns of allocation. We found that NPP per individual of foliage (Gfol), stem and branches (Gstem), coarse roots (Gcroot) and fine roots (Gfroot) in individual trees is largely explained (r2 = 67-91%) by the magnitude of total NPP per individual (G). Gfol scales with G isometrically, meaning it is a fixed fraction of G ( 25%). Root-shoot trade-offs were manifest as a slow decline in Gfroot, as a fraction of G, from 50% to 25% as stands increased in biomass, with Gstem and Gcroot increasing as a consequence. These results indicate that a functional trade-off between aboveground and belowground allocation is essentially captured by variations in G, which itself is largely governed by stand biomass and only secondarily by site-specific resource availability. We argue that forests are characterized by strong competition for light, observed as a race for individual trees to ascend by increasing partitioning toward wood, rather than by growing more leaves, and that this competition stronglyconstrains the allocational plasticity that trees may be capable of. The residual variation in partitioning was not related to climatic or edaphic factors, nor did plots with nutrient or water additions show a pattern of partitioning distinct from that predicted by G alone. These findings leverage short-term process studies of the terrestrial carbon cycle to improve decade-scale predictions of biomass accumulation in forests. An algorithm for calculating partitioning in land-surface models is presented.

Seasonal coupling of canopy structure and function in African tropical forests and its environmental controls

Tropical forests provide important ecosystem services in maintaining biodiversity, sequestering carbon and regulating climate regionally and globally. Climate triggers the seasonal transitions of vegetation structure and function in tropical forests. In turn, the seasonal cycles of structure and function in tropical forests feed back to the climate system through the control of land-atmosphere exchange of carbon, water and energy fluxes. Large uncertainties exist in the carbon and water budgets of tropical forests, and environmental controls on phenology are among the least understood factors. Although field studies have identified patterns in the environmental controls on local-scale species-level phenology in the tropics, there is little consensus on large-scale top-down environmental controls on whole-ecosystem seasonality. In this paper, we use both optical and microwave remote sensing to investigate the seasonality of vegetation canopy structure and function in three distinct tropical African forest types, and identify environmental triggers or controls of their variability. For most tropical forests that have a closed canopy and high leaf biomass, optical remote sensing (e.g., vegetation indices) captures canopy photosynthetic capacity (i.e., canopy function), while small-wavelength microwave remote sensing characterizes the leaf biomass and leaf water content of the upper canopy (i.e., canopy structure). Our results reveal a strong coupling of canopy structure with canopy function in the tropical deciduous forests and woody savannas, and their seasonalities are both controlled by precipitation rather than solar radiation. By contrast, tropical evergreen forests in Africa exhibit a decoupling of canopy structure from canopy function revealed by different sensors: canopy photosynthetic capacity shown by the optical remote sensing is linked to the seasonal variation of precipitation, while microwave remote sensing captures semi-annual leaf-flushing that is synchronous with peak insolation intensity at the top of the atmosphere, which is bimodal. The differential coupling of canopy structure and function in tropical forests observed from remote sensing highlights differences inherent in distinct vegetation types within the tropics that may originate in the different life histories of their respective floras. This satellite-based finding encourages more field-based studies to clarify the interpretation of these large scale patterns.

Detecting Tree-like Multicellular Life on Extrasolar Planets

Over the next two decades, NASA and ESA are planning a series of space-based observatories to find Earth-like planets and determine whether life exists on these planets. Previous studies have assessed the likelihood of detecting life through signs of biogenic gases in the atmosphere or a red edge. Biogenic gases and the red edge could be signs of either single-celled or multicellular life. In this study, we propose a technique with which to determine whether tree-like multicellular life exists on extrasolar planets. For multicellular photosynthetic organisms on Earth, competition for light and the need to transport water and nutrients has led to a tree-like body plan characterized by hierarchical branching networks. This design results in a distinct bidirectional reflectance distribution function (BRDF) that causes differing reflectance at different sun/view geometries. BRDF arises from the changing visibility of the shadows cast by objects, and the presence of tree-like structures is clearly distinguishable from flat ground with the same reflectance spectrum. We examined whether the BRDF could detect the existence of tree-like structures on an extrasolar planet by using changes in planetary albedo as a planet orbits its star. We used a semi-empirical BRDF model to simulate vegetation reflectance at different planetary phase angles and both simulated and real cloud cover to calculate disk and rotation-averaged planetary albedo for a vegetated and non-vegetated planet with abundant liquid water. We found that even if the entire planetary albedo were rendered to a single pixel, the rate of increase of albedo as a planet approaches full illumination would be comparatively greater on a vegetated planet than on a non-vegetated planet. Depending on how accurately planetary cloud cover can be resolved and the capabilities of the coronagraph to resolve exoplanets, this technique could theoretically detect tree-like multicellular life on exoplanets in 50 stellar systems.

The impact of large animal extinctions on nutrient fluxes in early river valley civilizations

Urbanization began independently in four river valley civilizations ∼3,500–5,000 years before the present (ybp) in fertile river valleys that originally had free-ranging large animals, including elephants, that eventually went locally extinct. Such large animals are disproportionally important in the lateral spread of nutrients away from nutrient concentration gradients common near floodplains, and the local extinction of the animals would have reduced this flow of nutrients into surrounding regions. Prior to the use of manure as a fertilizer, this natural spread of nutrients would have increased productivity and food yield, and its absence would have immediately decreased fertility to regions outside the floodplains. Here we calculate this changing nutrient flux using a “random walk” model and estimate that phosphorus (P) concentrations in the vegetation were reduced by >40% outside the floodplain following the loss of these animals and the process could take between 840 and 6,800 years depending on the ...