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Examples of stained root cross sections (A and C) and their corresponding xylem vessels (B and D, extracted in ImageJ) for one tree (A and B: Vachellia exuvialis) and one grass (C and D: Melinis repens) species from a South African lowveld savanna ecosystem grown under greenhouse conditions.

Examples of stained root cross sections (A and C) and their corresponding xylem vessels (B and D, extracted in ImageJ) for one tree (A and B: Vachellia exuvialis) and one grass (C and D: Melinis repens) species from a South African lowveld savanna ecosystem grown under greenhouse conditions.

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Article
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PREMISE: Belowground functional traits play a significant role in determining plant water use strategies and plant performance, but we lack data on root traits across communities, particularly in the tropical savanna biome, where vegetation dynamics are hypothesized to be strongly driven by tree–grass functional differences in water use. METHODS: W...

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... walls. This combination of dyes allowed us to highlight lignified tissue in xylem vessel walls (red) and cellulosic phloem cell walls (green), respectively ( Ma et al., 1993). We photographed all root sections present in each slide using a Leica DM750 binocular microscope (Leica Microsystems, Wetzlar, Germany) at both 4× and 10× magnifications (Fig. ...
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... used ImageJ to identify, measure, and count individual xylem vessels (e.g., Fig. 1) and the root diameter of each root cross section. We acknowledge that, barring actual observations of water flow through vessels (e.g., through staining), it is difficult to differentiate xylem vessels that play a meaningful role in transport from those that do not. Here, we focused on larger metaxylem vessels ( Kim et al., 2014), ...
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... final analysis included 539 individual root cross sections ( Fig. 1) distributed across 181 of the original 197 plants (median number of cross sections per plant = 3, range = 1-4). Of the initial group, 14 individual plants died before harvest, and two sample vials were labeled incorrectly, but all of the initial species/subspecies were represented in the final collection for analysis (Appendix S1). ...

Citations

... This work illustrated tradeoffs in safety versus efficiency of water transport in root microanatomy that predicted whole plant growth traits for perennial grasses [172]. Based on these observations, subsequent studies have highlighted how the internal root structure sets a foundation for the whole root system function [116,173,119]. Relationships between root microanatomy and aboveground physiology / growth vary by within communities [119], plant functional type [173] and phylogeny [167] and are an active topic of investigation. ...
... Based on these observations, subsequent studies have highlighted how the internal root structure sets a foundation for the whole root system function [116,173,119]. Relationships between root microanatomy and aboveground physiology / growth vary by within communities [119], plant functional type [173] and phylogeny [167] and are an active topic of investigation. Because microanatomical images of roots require more preparation time than whole root systems, they have been utilized much less than other traits. ...
Chapter
Long before the term ‘critical zone’ (CZ) was coined to encompass Earth’s biological and geological features from the top of the vegetative canopy to the depths of circulating groundwater, many scientists have recognized that both biotic and abiotic actors are centrally important for understanding many of Earth’s most fundamental processes. Contemporary CZ scientists continue this legacy. We describe findings that emphasize how life, emphasizing vegetation and microbes, responds to and shapes the physical environment in which it persists, yielding feedbacks for Earth’s climate, primarily through modifications to hydrologic functioning. We focus on the interactions of biota and the physical and chemical features of soil pedons and landscapes as they drive ecosystem-scale hydrologic fluxes. We focus on hydrologically-relevant features because of the long history of individual disciplines telling us about the large-scale importance of these processes, and because of emerging research highlighting the importance of the intersection of these disciplines for projecting future ecosystem functioning on a rapidly changing Earth. The knowledge we spotlight reveals Earth’s CZ as a fundamentally ecological problem.
... In particular, whereas in mesic savannas plants compete for water and nutrients, in drier savannas, the positive effect of the shade may outweigh the negative effects of direct competition for water (Dohn et al., 2013). Because grasses are more efficient users of soil moisture than are trees in mesic environments (as has been shown in mesic environments; Wargowsky et al., 2021;Xu et al., 2015), one would expect that tree-grass competition would be stronger under scenarios of high productivity and soil water availability. ...
... Overall, we showed that the grass layer constitutes a strong filter to tree seedling survival. This phenomenon is primarily attributed to below-ground resource competition during the establishment phase, when the roots of tree seedlings and grasses overlap (Aerts et al., 1991;McConnaughay & Bazzaz, 1992;Cramer et al., 2010Cramer et al., , 2012February et al., 2013;Wakeling et al., 2015;Xu et al., 2015;Pillay & Ward, 2021;Wargowsky et al., 2021). In savannas the great root biomass of tussocks and prostrate grasses may occupy a large proportion of the available rooting space that may limit the establishment of tree seedling roots by spatial exclusion (Knoop & Walker, 1985;McConnaughay & Bazzaz, 1992;Pillay & Ward, 2021). ...
Article
Questions How does the grass layer affect seedlings across large environmental gradients in savannas? Location Savanna sites in Argentina, Tanzania, and South Africa. Methods We carried out a joint analysis of three grass removal experiments in which seedlings of various Fabaceae species were transplanted into plots with native grass and companion plots where grass had been removed. First, we estimated the effect of grasses on tree seedling mortality and seedling growth rate at each site. Then, we used the resulting coefficient estimates from site‐level models to examine the impact of two climate (monthly precipitation and aridity index) and two soil (soil organic carbon content and clay content) variables on the direction and magnitude of the grass effects. Results Grasses increased the risk of mortality, but there was no evidence for a global effect of grasses on tree seedling rate of height growth. The best model fit indicated a high mortality risk of tree seedlings in response to grasses at intermediate aridity index values. No other climate or soil variable influenced tree seedling survival or growth (monthly precipitation, soil organic carbon content and clay content). Conclusions Our results support the notion that the grass layer consistently creates a bottleneck to tree seedling establishment in African and South American savannas beyond climate and soil conditions, mainly by affecting tree seedling survival. The negative effect of grasses on seedling survival was lower in dry conditions compared to intermediate aridity levels. These results suggest that grass–seedling interaction is less intense in drier conditions, possibly due to reduced total grass biomass, which leads to decreased site evapotranspiration and improved soil water retention capacity.
... (3) How do C. drummondii hydraulics (K shoot , K root , K plant , and stem P 50 ) vary under experimental fire and drought? Given that grasses have fibrous shallow root systems that are efficient at water uptake Wargowsky et al. 2021), we hypothesized that A. gerardii would have greater K root than C. drummondii. However, because the deep root system of C. drummondii relies on stable water while the shallow root system of A. gerardii routinely experiences fluctuations in water availability, we hypothesized that C. drummondii hydraulics would Content courtesy of Springer Nature, terms of use apply. ...
... This result is not surprising given that C 4 grasses typically have dense, fibrous root systems that can maximize water uptake in resource-limited systems . In fact, C 4 grasses are often characterized as "aggressive" users of water because they exhibit root traits that allow them to sustain higher transpiration and growth rates than woody plants under wet conditions (Xu et al. 2015;Wargowsky et al. 2021;Belovitch et al. 2023). Consistent with this notion, previous work at this site has shown that grass root biomass and total root length are greatest within the top 20 cm of soil , and that grass root biomass is significantly greater in shallower soil compared to woody root biomass (R. Keen, unpublished data). ...
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Whole-plant hydraulics provide important information about responses to water limitation and can be used to understand how plant communities may change in a drier climate when measured on multiple species. Here, we measured above- and belowground hydraulic traits in Cornus drummondii, an encroaching shrub within North American tallgrass prairies, and Andropogon gerardii, a dominant C4 grass, to assess the potential hydraulic responses to future drought as this region undergoes woody expansion. Shelters that reduced precipitation by 50% and 0% were built over shrubs and grasses growing in sites that are burned at 1-year and 4-year frequencies. We then measured aboveground (Kshoot), belowground (Kroot), and whole-plant maximum hydraulic conductance (Kplant) in C. drummondii and Kroot in A. gerardii. We also measured vulnerability to embolism (P50) in C. drummondii stems. Overall, we show that: (1) A. gerardii had substantially greater Kroot than C. drummondii; (2) belowground hydraulic functioning was linked with aboveground processes; (3) above- and belowground C. drummondii hydraulics were not negatively impacted by the rainfall reductions imposed here. These results suggest that a multi-year drought will not ameliorate rates of woody expansion and highlight key differences in aboveground and belowground hydraulics for dominant species within the same ecosystem.
... Species with large vessels are also likely to have a high proportion of axial parenchyma surrounding these vessels (Morris et al., 2018). Woody plants in tropical savannas have rather narrow vessels and a relatively high resistance to xylem embolism (Chen et al., 2021;Wargowsky et al., 2021). Interestingly, the width and length of cutopen vessels in stem segments has been shown to affect the lipid concentration in extracted xylem sap (Guan et al., 2022;Schenk et al., 2021). ...
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Lipids may play an important role in preventing gas embolisms by coating nanobubbles in xylem sap. Few studies on xylem sap lipids have been reported for temperate plants, and it remain unclear whether sap lipids have adaptational significance in tropical plants. In this study, we quantify the lipid composition of xylem sap for angiosperm species from a tropical savanna (seven species) and a seasonal rainforest (five species) using mass spectrometry. We found that all twelve species studied contained lipids in their xylem sap, including galactolipids, phospholipids and triacylglycerol, with a total lipid concentration ranging from 0.09 to 0.26 nmol/L. There was no difference in lipid concentration or composition between plants from the two sites, and the lipid concentration was negatively related to species’ open vessel volume. Furthermore, savanna species showed little variation in lipid composition between the dry and the rainy season. These results support the hypothesis that xylem sap lipids are derived from the cytoplasm of individual conduit cells, remain trapped inside individual conduits, and undergo few changes in composition over consecutive seasons. A xylem sap lipidomic data set, which includes 12 tropical tree species from this study and 11 temperate tree species from literature, revealed no phylogenetic signals in lipid composition for these species. This study fills a knowledge gap in the lipid content of xylem sap in tropical trees and provides additional support for their common distribution in xylem sap of woody angiosperms. It appears that xylem sap lipids have no adaptive significance.
... To estimate plant mass gain, we needed an estimate of initial and final belowground mass, which we did not quantify in this experiment. We therefore used measurements of root mass ratio for our study species obtained in a separate glasshouse experiment (Wargowsky et al., 2021) to estimate the initial and total final mass of each plant on the basis of initial and final shoot mass. To test for tree-grass differences in whole-plant WUE, RGR, and Ψ osm , we used mixed models implemented with the lme function in the NLME package (Pinheiro & Bates, 2000) treating species as a random effect. ...
Article
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Models of tree–grass coexistence in savannas make different assumptions about the relative performance of trees and grasses under wet vs dry conditions. We quantified transpiration and drought tolerance traits in 26 tree and 19 grass species from the African savanna biome across a gradient of soil water potentials to test for a trade‐off between water use under wet conditions and drought tolerance. We measured whole‐plant hourly transpiration in a growth chamber and quantified drought tolerance using leaf osmotic potential (Ψosm). We also quantified whole‐plant water‐use efficiency (WUE) and relative growth rate (RGR) under well‐watered conditions. Grasses transpired twice as much as trees on a leaf‐mass basis across all soil water potentials. Grasses also had a lower Ψosm than trees, indicating higher drought tolerance in the former. Higher grass transpiration and WUE combined to largely explain the threefold RGR advantage in grasses. Our results suggest that grasses outperform trees under a wide range of conditions, and that there is no evidence for a trade‐off in water‐use patterns in wet vs dry soils. This work will help inform mechanistic models of water use in savanna ecosystems, providing much‐needed whole‐plant parameter estimates for African species.
... This finding, however, is based on modeling work that, similar to Holdo (2013), puts aside tree-grass differences in root transport capacity, drought tolerance, transpiration, and water use efficiency to focus exclusively on rooting differences (Kulmatiski & Beard, 2022). Importantly, grasses outperform trees in all of these metrics (Wargowsky et al., 2021;O'Keefe et al., 2022;Belovitch et al., unpublished), thus helping tilt the competitive advantage toward grass dominance. We argue that the two-layer model is alive and well but that it needs to incorporate the full range of differences in tree and grass ecohydrological traits (Ward et al., 2013). ...
... There is ample evidence for grasses being competitively dominant to trees when competing within the same soil layers, across a wide range of soil moisture conditions (Walker et al., 1981;Walker & Noy-Meir, 1982;February et al., 2013;Campbell & Holdo, 2017). Grasses have finer roots than trees (Nippert et al., 2012;Ma et al., 2018;O'Keefe et al., 2022), resulting in a higher specific root length and greater absorptive surface area per volume of soil (Ma et al., 2018), higher fine-root conductivity (Wargowsky et al., 2021), and whole-plant transpiration rates per unit mass (Belovitch et al., unpublished). The root diameter imposes a trade-off: grasses have a larger absorptive capacity than trees in topsoil fine roots, but trees have a greater capacity for longdistance (i.e. ...
Article
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Savannas cover a significant fraction of the Earth's land surface. In these ecosystems, C3 trees and C4 grasses coexist persistently, but the mechanisms explaining coexistence remain subject to debate. Different quantitative models have been proposed to explain coexistence, but these models make widely contrasting assumptions about which mechanisms are responsible for savanna persistence. Here, we show that no single existing model fully captures all key elements required to explain tree–grass coexistence across savanna rainfall gradients, but many models make important contributions. We show that recent empirical work allows us to combine many existing elements with new ideas to arrive at a synthesis that combines elements of two dominant frameworks: Walter's two‐layer model and demographic bottlenecks. We propose that functional rooting separation is necessary for coexistence and is the crux of the coexistence problem. It is both well‐supported empirically and necessary for tree persistence, given the comprehensive grass superiority for soil moisture acquisition. We argue that eventual tree dominance through shading is precluded by ecohydrological constraints in dry savannas and by fire and herbivores in wet savannas. Strong asymmetric grass–tree competition for soil moisture limits tree growth, exposing trees to persistent demographic bottlenecks.
... For trees, we found a significant phylogenetic signal 229 only in the case of BI, suggesting that branching patterns may be more strongly evolutionarily 230 conserved than other morphological traits (Fig. 5). This result differs from the phylogenetic 231 analysis of the vessel anatomical traits, which found a significant phylogenetic signal across 232 multiple traits in trees (Wargowsky et al., 2021). The first two axes of the PCA captured 233 approximately 66% of the variation in the data, with PC1 and PC2 representing 49.4% and 234 ...
... ., 2562020;Xu et al., 2015). In conjunction with a companion study showing significantly higher 257 theoretical water transport capacity per root in the same cohort of plants(Wargowsky et al., 258 2021), our results support the notion of grasses being more efficient in terms of their ability to 259 rapidly deplete soil moisture in the rooting zone.Wargowsky et al., (2021) found systematic 260 differences in rooting vessel anatomy between trees and grasses, with grasses exhibiting greater 261 predicted conductivities and larger fine-root xylem vessels than trees, allowing them to transport 262 water more efficiently. The combination of high root length per unit mass and larger vessels 263 allows grasses a ...
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Purpose Soil moisture availability is a key driver of the relative abundance of trees and grasses in savannas. Fine root morphology influences water acquisition and transport, yet differences in fine root traits between trees and grasses have not been comprehensively quantified across an entire suite of coexisting tree and grass species. Methods We grew individuals of 21 tree and 18 grass species from a Lowveld savanna ecosystem in South Africa under greenhouse conditions and characterized six root traits: root diameter, branching intensity, specific root length, root length to leaf area ratio, distal to total root length ratio, and root length to plant mass ratio. We conducted a PCA to evaluate whether some morphological root traits can act as predictive traits for other, more difficult to measure traits. Results We found strong differences between trees and grasses across all six root morphological traits, particularly root diameter and branching intensity. Trees had thicker roots than grasses, while grasses had higher specific root length, greater branching intensity, a greater relative investment in distal roots, and a higher ratio of root length to plant mass than trees. Despite strong species-level effects on trait values, we found little evidence of phylogenetic signals in trait values for either trees or grasses. Conclusion We found strong evidence of significant morphological differences among savanna trees and grasses. Our results are consistent with the observation that grasses can outperform trees when competing directly for belowground resources.
... The fast-slow trade-off implies that a fine-tuned coordination between above and belowground organs should exist (Reich 2014). Species with high gas exchange rates at the leaf would require efficient roots and xylem to ensure a continuous water and nutrient supply in comparison to species with lower metabolic rates de la Riva et al. 2018;Wargowsky et al. 2021). However, evidence supporting this whole plant coordination displays no clear pattern suggesting that the complex root functions may respond to other factors as complex abiotic stresses and, perhaps, phylogenetic constraints (Freschet et al. 2010;de la Riva et al. 2016;Kramer-Walter et al. 2016;Weemstra et al. 2016;Liese et al. 2017;Messier et al. 2017;Carvajal et al. 2019;Hu et al. 2019;Shen et al. 2019;Delpiano et al. 2020). ...
Article
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Key message Oak species displayed high interspecific functional trait variation. The resource use strategy among oaks both at the above and belowground organs was guided by the fast-slow continuum. AbstractPlant functional ecology has focused on the study of functional strategies and general patterns of trait covariation. Mostly, studies intend to elucidate how plants cope with resource capture both at the above and belowground organs and to understand how the capacity for resource gain relates with the species distribution. American oaks are an interesting and important tree clade, they radiated into diverse environments outside temperate regions implying the development of adaptations to persist under different environmental regimes. Therefore, we explored patterns of differentiation in functional traits related with the capacity for resource use in 3-month seedlings of ten Mexican oak species representative from semiarid, temperate and subtropical montane regions. We examined the fast–slow trade-off and its importance in species differentiation on both above and belowground organs. Additionally, we investigated how resource acquisition strategy of the species was related with the environmental conditions experienced in their habitats. We found a significant differentiation in both above and belowground traits, and in both cases oak species segregated along the fast–slow continuum. We found only a few significant trait-by-trait relationships, implying a weak coordination among aerial and subterranean organs. Additionally, species from sites with higher precipitation seasonality had a higher root growth, and species from humid sites had larger leaves. These findings highlight important functional variation among oak seedlings which was related with the climatic conditions encompassed along their native geographic range.
... While previous research has indicated that anatomical traits can influence/constrain physiological responses to changes in water availability (Christin et al. 2013;Guha et al. 2018;Edson-Chaves and Graciano-Ribeiro 2018;Wargowsky et al. 2021), a few studies have analyzed physiology, stoichiometry, and anatomy of the same leaf across multiple years and locations. The importance of this sampling technique allowed us to analyze relationships of both functional trait mean and variability (CV) (Figs. 4, S1; Tables S1, S2). ...
Article
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Grassland ecosystems are historically shaped by climate, fire, and grazing which are essential ecological drivers. These grassland drivers influence morphology and productivity of grasses via physiological processes, resulting in unique water and carbon-use strategies among species and populations. Leaf-level physiological responses in plants are constrained by the underlying anatomy, previously shown to reflect patterns of carbon assimilation and water-use in leaf tissues. However, the magnitude to which anatomy and physiology are impacted by grassland drivers remains unstudied. To address this knowledge gap, we sampled from three locations along a latitudinal gradient in the mesic grassland region of the central Great Plains, USA during the 2018 (drier) and 2019 (wetter) growing seasons. We measured annual biomass and forage quality at the plot level, while collecting physiological and anatomical traits at the leaf-level in cattle grazed and ungrazed locations at each site. Effects of ambient drought conditions superseded local grazing treatments and reduced carbon assimilation and total productivity in A. gerardii . Leaf-level anatomical traits, particularly those associated with water-use, varied within and across locations and between years. Specifically, xylem area increased when water was more available (2019), while xylem resistance to cavitation was observed to increase in the drier growing season (2018). Our results highlight the importance of multi-year studies in natural systems and how trait plasticity can serve as vital tool and offer insight to understanding future grassland responses from climate change as climate played a stronger role than grazing in shaping leaf physiology and anatomy.
Article
Savannas are complex ecosystems where multiple growth forms, including grasses, trees, and subshrubs, coexist through intricate ecological interactions. Understanding the mechanisms that promote this coexistence is key to conserving savanna biodiversity. This study investigated the effects of grass competition on the survival and growth of trees and subshrubs, as well as the interactions between these two growth forms. Using three species of trees and three species of subshrubs, we conducted a greenhouse experiment to assess how competition between trees and subshrubs is influenced by the presence of grass. We found that grass competition significantly reduced the survival of tree seedlings, while subshrubs were unaffected. When trees and subshrubs competed directly, subshrub biomass was reduced, but only in the absence of grass. Tree seedling biomass was not affected by subshrubs, but was negatively impacted by grass in the absence of subshrubs. Both root and stem biomass of trees and subshrubs were reduced by grass competition; however, this effect was mitigated when grasses, subshrubs, and trees competed simultaneously. These results indicate that when grasses, subshrubs, and trees compete together, the intensity of competition is reduced, promoting coexistence and contributing to the balance of growth forms in savanna ecosystems. While fire is an important factor in savanna dynamics, our study emphasizes the critical role of competition in maintaining this balance. Future studies should explore how fire and competition interact to further our understanding of biodiversity and ecosystem function in Neotropical savannas. Abstract in Portuguese is available with online material.