& Key message Abundant Neotropical canopy-tree species are more resistant to drought-induced branch embolism than what is currently admitted. Large hydraulic safety margins protect them from hydraulic failure under actual drought conditions. & Context Xylem vulnerability to embolism, which is associated to survival under extreme drought conditions, is being increasingly studied in the tropics, but data on the risk of hydraulic failure for lowland Neotropical rainforest canopy-tree species, thought to be highly vulnerable, are lacking. & Aims The purpose of this study was to gain more knowledge on species drought-resistance characteristics in branches and leaves and the risk of hydraulic failure of abundant rainforest canopy-tree species during the dry season. & Methods We first assessed the range of branch xylem vulnerability to embolism using the flow-centrifuge technique on 1-mlong sun-exposed branches and evaluated hydraulic safety margins with leaf turgor loss point and midday water potential during normal-and severe-intensity dry seasons for a large set of Amazonian rainforest canopy-tree species. & Results Tree species exhibited a broad range of embolism resistance, with the pressure threshold inducing 50% loss of branch hydraulic conductivity varying from − 1.86 to − 7.63 MPa. Conversely, we found low variability in leaf turgor loss point and dry season midday leaf water potential, and mostly large, positive hydraulic safety margins.
Hydraulic segmentation at the stem-leaf transition predicts higher hydraulic resistance in leaves than in stems. Vulnerability segmentation, however, predicts lower embolism resistance in leaves. Both mechanisms should theoretically favour runaway embolism in leaves to preserve expensive organs such as stems, and should be tested for any potential coordination. We investigated the theoretical leaf-specific conductivity based on an anatomical approach to quantify the degree of hydraulic segmentation across 21 tropical rainforest tree species. Xylem resistance to embolism in stems (flow-centrifugation technique) and leaves (optical visualization method) was quantified to assess vulnerability segmentation. We found a pervasive hydraulic segmentation across species, but with a strong variability in the degree of segmentation. Despite a clear continuum in the degree of vulnerability segmentation, eight species showed a positive vulnerability segmentation (leaves less resistant to embolism than stems), whereas the remaining species studied exhibited a negative or no vulnerability segmentation. The degree of vulnerability segmentation was positively related to the degree of hydraulic segmentation, such that segmented species promote both mechanisms to hydraulically decouple leaf xylem from stem xylem. To what extent hydraulic and vulnerability segmentation determine drought resistance requires further integration of the leaf-stem transition at the whole-plant level, including both xylem and outer xylem tissue.
Warmer and drier climates over Amazonia have been predicted for the next century with expected changes in regional water and carbon cycles. We examined the impact of interannual and seasonal variations in climate conditions on ecosystem-level evapotranspiration (ET) and water use efficiency (WUE) to determine key climatic drivers and anticipate the response of these ecosystems to climate change. We used daily climate and eddyflux data recorded at the Guyaflux site in French Guiana from 2004 to 2014. ET and WUE exhibited weak interannual variability. The main climatic driver of ET and WUE was global radiation (Rg), but relative extractable water (REW) and soil temperature (Ts) did also contribute. At the seasonal scale, ET and WUE showed a modal pattern driven by Rg, with maximum values for ET in July and August and for WUE at the beginning of the year. By removing radiation effects during water depleted periods, we showed that soil water stress strongly reduced ET. In contrast, drought conditions enhanced radiation-normalized WUE in almost all the years, suggesting that the lack of soil water had a more severe effect on ecosystem evapotranspiration than on photosynthesis. Our results are of major concern for tropical ecosystem modeling because they suggest that under future climate conditions, tropical forest ecosystems will be able to simultaneously adjust CO2 and H2O fluxes. Yet, for tropical forests under future conditions, the direction of change in WUE at the ecosystem scale is hard to predict, since the impact of radiation on WUE is counterbalanced by adjustments to soil water limitations. Developing mechanistic models that fully integrate the processes associated with CO2 and H2O flux control should help researchers understand and simulate future functional adjustments in these ecosystems.
Results from laboratory feeding experiments have shown that elevated atmospheric carbon dioxide can affect interactions between plants and insect herbivores, primarily through changes in leaf nutritional quality occurring at elevated CO. Very few data are available on insect herbivory in plant communities where insects can choose among species and positions in the canopy in which to feed. Our objectives were to determine the extent to which CO-induced changes in plant communities and leaf nutritional quality may affect herbivory at the level of the entire canopy. We introduced equivalent populations of fourth instar Spodoptera eridania, a lepidopteran generalist, to complex model ecosystems containing seven species of moist tropical plants maintained under low mineral nutrient supply. Larvae were allowed to feed freely for 14 days, by which time they had reached the seventh instar. Prior to larval introductions, plant communities had been continuously exposed to either 340 μl CO l or to 610 μl CO l for 1.5 years. No major shifts in leaf nutritional quality [concentrations of N, total non-structural carbohydrates (TNC), sugar, and starch; ratios of: C/N, TNC/N, sugar/N, starch/N; leaf toughness] were observed between CO treatments for any of the species. Furthermore, no correlations were observed between these measures of leaf quality and leaf biomass consumption. Total leaf area and biomass of all plant communities were similar when caterpillars were introduced. However, leaf biomass of some species was slightly greater-and for other species slightly less (e.g. Cecropia peltata)-in communities exposed to elevated CO. Larvae showed the strongest preference for C. peltata leaves, the plant species that was least abundant in all communites, and fed relatively little on plants species which were more abundant. Thus, our results indicate that leaf tissue quality, as described by these parameters, is not necessarily affected by elevated CO under relatively low nutrient conditions. Hence, the potential importance of CO-induced shifts in leaf nutritional quality, as determinants of herbivory, may be overestimated for many plant communities growing on nutrient-poor sites if estimates are based on traditional laboratory feeding studies. Finally, slight shifts in the abundance of leaf tissue of various species occurring under elevated CO will probably not significantly affect herbivory by generalist insects. However, generalist insect herbivores appear to become more dependent on less-preferred plant species in cases where elevated CO results in reduced availability of leaves of a favoured plant species, and this greater dependency may eventually affect insect populations adversely.
Summary Drought‐induced xylem embolism is considered to be one of the main factors driving mortality in woody plants worldwide. Although several structure–functional mechanisms have been tested to understand the anatomical determinants of embolism resistance, there is a need to study this topic by integrating anatomical data for many species. We combined optical, laser, and transmission electron microscopy to investigate vessel diameter, vessel grouping, and pit membrane ultrastructure for 26 tropical rainforest tree species across three major clades (magnoliids, rosiids, and asteriids). We then related these anatomical observations to previously published data on drought‐induced embolism resistance, with phylogenetic analyses. Vessel diameter, vessel grouping, and pit membrane ultrastructure were all predictive of xylem embolism resistance, but with weak predictive power. While pit membrane thickness was a predictive trait when vestured pits were taken into account, the pit membrane diameter‐to‐thickness ratio suggests a strong importance of the deflection resistance of the pit membrane. However, phylogenetic analyses weakly support adaptive coevolution. Our results emphasize the functional significance of pit membranes for air‐seeding in tropical rainforest trees, highlighting also the need to study their mechanical properties due to the link between embolism resistance and pit membrane diameter‐to‐thickness ratio. Finding support for adaptive coevolution also remains challenging.
Tropical canopies are complex, with multiple canopy layers and pronounced gap dynamics contributing to their high species diversity and productivity. An important reason for this complexity is the large variation in shade tolerance among different tree species. At present, we lack a clear understanding of which plant traits control this variation, e.g., regarding the relative contributions of whole-plant versus leaf traits or structural versus physiological traits. We investigated a broad range of traits in six tropical montane rainforest tree species with different degrees of shade tolerance, grown under three different radiation regimes (under the open sky or beneath sparse or dense canopies). The two distinct shade-tolerant species had higher fractional biomass in leaves and branches while shade-intolerant species invested more into stems, and these differences were greater under low radiation. Leaf respiration and photosynthetic light compensation point did not vary with species shade tolerance, regardless of radiation regime. Leaf temperatures in open plots were markedly higher in shade-tolerant species due to their low transpiration rates and large leaf sizes. Our results suggest that interspecific variation in shade tolerance of tropical montane trees is controlled by species differences in whole-plant biomass allocation strategy rather than by difference in physiological leaf traits determining leaf carbon balance at low radiation.
Differences in photosynthetic capacity among tree species and tree functional types are currently assumed to be largely driven by variation in leaf nutrient content, particularly nitrogen (N). However, recent studies indicate that leaf N content is often a poor predictor of variation in photosynthetic capacity in tropical trees. In this study, we explored the relative importance of area-based total leaf N content (N tot) and within-leaf N allocation to photosynthetic capacity versus light-harvesting in controlling the variation in photosynthetic capacity (i.e. V cmax , J max) among mature trees of 12 species belonging to either early (ES) or late successional (LS) groups growing in a tropical montane rainforest in Rwanda, Central Africa. Photosynthetic capacity at a common leaf temperature of 25˚C (i.e. maximum rates of Rubisco carboxylation, V cmax25 and of electron transport, J max25) was higher in ES than in LS species (+ 58% and 68% for V cmax25 and J max25 , respectively). While N tot did not significantly differ between successional groups, the photosynthetic dependency on N tot was markedly different. In ES species, V cmax25 was strongly and positively related to N tot but this was not the case in LS species. However, there was no significant trade-off between relative leaf N investments in compounds maximizing photosynthetic capacity versus compounds maximizing light harvesting. Both leaf dark respiration at 25˚C (+ 33%) and, more surprisingly, apparent photosynthetic quantum yield (+ 35%) was higher in ES than in LS species. Moreover, R d25 was positively related to N tot for both ES and LS species. Our results imply that efforts to quantify carbon fluxes of tropical montane rainforests would be improved if they considered contrasting within-leaf N allocation and photosynthetic N tot dependencies between species with different successional strategies.
Embolism spreading in xylem is an important component of plant drought resistance. Since embolism resistance has been shown to be mechanistically linked to pit membrane characters in stem xylem, we speculate that similar mechanisms account for leaf xylem. We conducted transmission electron microscopy to investigate pit membrane characters in leaf xylem across 18 Neotropical tree species. We also conducted gold perfusion and polar lipid detection experiments on three species covering the full range of leaf embolism resistance. We then related these observations to previously published data on embolism resistance of leaf xylem. We also incorporated previously published data on stem embolism resistance and stem xylem pit membranes to investigate the link between vulnerability segmentation (i.e., difference in embolism resistance) and leaf-stem anatomical variation. Pit membrane thickness (Tpm,max) and the pit membrane thickness-to-diameter ratio (Tpm,max/Dpm) were predictive of leaf embolism resistance, especially when vestured pits were taken into account. Variation in Tpm,max/Dpm was the only trait predictive of vulnerability segmentation between leaves and stems. Gold particles of 5 and 10 nm infiltrated pit membranes in three species, while the entry of 50-nm particles was blocked. Moreover, polar lipids were associated with inner conduit walls and pits. Our results suggest that mechanisms related to embolism spreading are determined by pit membrane thickness, pore constrictions (i.e., the narrowest bottlenecks along pore pathways), and lipid surfactants, which are largely similar between leaf and stem xylem and between temperate and tropical trees. However, our mechanistic understanding of embolism propagation and the functional relevance of Tpm,max/Dpm remains elusive.
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