Coordination of pinna, petiole, and root anatomical traits in 24 tropical-subtropical fern species.

Ferns are primitive vascular plants with diverse morphologies and structures. Plant anatomical traits and their linkages can reflect adaptation to the environment; however, these remain are still poorly understood in ferns. The main objective of this study was to explore whether there was structural coordination among and within organs in fern species. We measured 16 hydraulically related anatomical traits of pinnae, petioles, and roots of 24 representative fern species from the tropical and subtropical forest understory and analyzed trait correlation networks. In addition, we examined phylogenetic signals for the anatomical traits and analyzed co-evolutionary relationships. These results indicated that stomatal density and all petiole anatomical traits exhibited significant phylogenetic signals. Evolutionary correlations were observed between the tracheid diameter and wall thickness of the petiole and between the water transport capacity of the petiole and stomatal density. Conversely, anatomical traits of roots (e.g., root diameter) showed no phylogenetic signals and were not significantly correlated with those of the pinnae and petioles, indicating a lack of structural coordination between the below- and above-ground organs. Unlike angiosperms, vein density is unrelated to stomatal density or pinna thickness in ferns. As root diameter decreased, the cortex-to-stele diameter ratio decreased significantly (enhanced water absorption) in angiosperms but remained unchanged in ferns. These differences lead to different responses of ferns to climate change and improve our knowledge of the water adaptation strategies of ferns.

Water storage capacity is inversely associated with xylem embolism resistance in tropical karst tree species.

Tropical karst habitats are characterized by limited and patchy soil, large rocky outcrops and porous substrates, resulting in high habitat heterogeneity and soil moisture fluctuations. Xylem hydraulic efficiency and safety can determine the drought adaptation and spatial distribution of woody plants growing in karst environments. In this study, we measured sapwood-specific hydraulic conductivity (Ks), vulnerability to embolism, wood density, saturated water content, and vessel and pit anatomical characteristics in the branch stems of 12 evergreen tree species in a tropical karst seasonal rainforest in southwestern China. We aimed to characterize the effects of structural characteristics on hydraulic efficiency and safety. Our results showed that there was no significant correlation between Ks and hydraulic safety across the tropical karst woody species. Ks was correlated with hydraulic vessel diameter (r = 0.80, P < 0.05) and vessel density (r = -0.60, P < 0.05), while the stem water potential at 50 and 88% loss of hydraulic conductivity (P50 and P88) were both significantly correlated with wood density (P < 0.05) and saturated water content (P = 0.052 and P < 0.05, respectively). High stem water storage capacity was associated with low cavitation resistance possibly because of its buffering the moisture fluctuations in karst environments. However, both Ks and P50/P88 were decoupled from the anatomical traits of pit and pit membranes. This may explain the lack of tradeoff between hydraulic safety and efficiency in tropical karst evergreen tree species. Our results suggest that diverse hydraulic trait combination may facilitate species coexistence in karst environments with high spatial heterogeneity.

Can leaf drought tolerance predict species abundance and its changes in tropical-subtropical forests?

Climate change has resulted in an increase in drought severity in the species-rich tropical and subtropical forests of southern China. Exploring the spatiotemporal relationship between drought-tolerance trait and tree abundance provides a means to elucidate the impact of droughts on community assembly and dynamics. In this study, we measured the leaf turgor loss point (πtlp) for 399 tree species from three tropical forest plots and three subtropical forest plots. The plot area was 1 ha and tree abundance was calculated as total basal area per hectare according to the nearest community census data. The first aim of this study was to explore πtlp abundance relationships in the six plots across a range of precipitation seasonality. Additionally, three of the six plots (two tropical forests and one subtropical forest) had consecutive community censuses data (12-22 years) and the mortality ratios and abundance year slope of tree species were analyzed. The second aim was to examine whether πtlp is a predictor of tree mortality and abundance changes. Our results showed that tree species with lower (more negative) πtlp were more abundant in the tropical forests with relative high seasonality. However, πtlp was not related to tree abundance in the subtropical forests with low seasonality. Moreover, πtlp was not a good predictor of tree mortality and abundance changes in both humid and dry forests. This study reveals the restricted role of πtlp in predicting the response of forests to increasing droughts under climate change.

Tree growth is correlated with hydraulic efficiency and safety across 22 tree species in a subtropical karst forest.

Karst forests are habitats in which access to soil water can be challenging for plants. Therefore, safe and efficient xylem water transport and large internal water storage may benefit tree growth. In this study, we selected 22 tree species from a primary subtropical karst forest in southern China and measured their xylem anatomical traits, saturated water content (SWC), hydraulic conductivity (Ks) and embolism resistance (P50). Additionally, we monitored growth of diameter at breast height (DBH) in 440 individual trees of various sizes over three consecutive years. Our objective was to analyze the relationships between xylem structure, hydraulic efficiency, safety, water storage and growth of karst tree species. The results showed significant differences in structure but not in hydraulic traits between deciduous and evergreen species. Larger vessel diameter, paratracheal parenchyma and higher SWC were correlated with higher Ks. Embolism resistance was not correlated with the studied anatomical traits, and no tradeoff with Ks was observed. In small trees (5-15 cm DBH), diameter growth rate (DGR) was independent of hydraulic traits. In large trees (>15 cm DBH), higher Ks and more negative P50 accounted for higher DGR. From lower to greater embolism resistance, the size-growth relationship shifted from growth deceleration to acceleration with increasing tree size in eight of the 22 species. Our study highlights the vital contributions of xylem hydraulic efficiency and safety to growth rate and dynamics in karst tree species; therefore, we strongly recommend their integration into trait-based forest dynamic models.

Correlations between leaf economics, mechanical resistance and drought tolerance across 41 cycad species.

BACKGROUND AND AIMS: We conducted a comprehensive analysis of the functional traits of leaves (leaflets) of cycads. The aim of this study was to clarify the functional divergence between the earlier origin Cycadaceae and the later differentiated Zamiaceae, and the differences in trait associations between cycads and angiosperms. METHODS: We selected 20 Cycadaceae species and 21 Zamiaceae species from the same cycad garden in South China, and measured their leaf structure, economic traits, mechanical resistance (Fp) and leaf water potential at the turgor loss point (πtlp). In addition, we compiled a dataset of geographical distribution along with climatic variables for these cycad species, and some leaf traits of tropical-sub-tropical angiosperm woody species from the literature for comparison. KEY RESULTS: The results showed significantly contrasting leaf trait syndromes between the two families, with Zamiaceae species exhibiting thicker leaves, higher carbon investments and greater Fp than Cycadaceae species. Leaf thickness (LT) and πtlp were correlated with mean climatic variables in their native distribution ranges, indicating their evolutionary adaptation to environmental conditions. Compared with the leaves of angiosperms, the cycad leaves were thicker and tougher, and more tolerant to desiccation. Greater Fp was associated with a higher structural investment in both angiosperms and cycads; however, cycads showed lower Fp at a given leaf mass per area or LT than angiosperms. Enhancement of Fp led to more negative πtlp in angiosperms, but the opposite trend was observed in cycads. CONCLUSIONS: Our results reveal that variations in leaf traits of cycads are mainly influenced by taxonomy and the environment of their native range. We also demonstrate similar leaf functional associations in terms of economics, but different relationships with regard to mechanics and drought tolerance between cycads and angiosperms. This study expands our understanding of the ecological strategies and likely responses of cycads to future climate change.

Co-ordination between leaf biomechanical resistance and hydraulic safety across 30 sub-tropical woody species.

BACKGROUND AND AIMS: Leaf biomechanical resistance protects leaves from biotic and abiotic damage. Previous studies have revealed that enhancing leaf biomechanical resistance is costly for plant species and leads to an increase in leaf drought tolerance. We thus predicted that there is a functional correlation between leaf hydraulic safety and biomechanical characteristics. METHODS: We measured leaf morphological and anatomical traits, pressure-volume parameters, maximum leaf hydraulic conductance (Kleaf-max), leaf water potential at 50 % loss of hydraulic conductance (P50leaf), leaf hydraulic safety margin (SMleaf), and leaf force to tear (Ft) and punch (Fp) of 30 co-occurring woody species in a sub-tropical evergreen broadleaved forest. Linear regression analysis was performed to examine the relationships between biomechanical resistance and other leaf hydraulic traits. KEY RESULTS: We found that higher Ft and Fp values were significantly associated with a lower (more negative) P50leaf and a larger SMleaf, thereby confirming the correlation between leaf biomechanical resistance and hydraulic safety. However, leaf biomechanical resistance showed no correlation with Kleaf-max, although it was significantly and negatively correlated with leaf outside-xylem hydraulic conductance. In addition, we also found that there was a significant correlation between biomechanical resistance and the modulus of elasticity by excluding an outlier. CONCLUSIONS: The findings of this study reveal leaf biomechanical-hydraulic safety correlation in sub-tropical woody species.

Leaf hydraulic safety margin and safety-efficiency trade-off across angiosperm woody species.

Leaf hydraulic conductance and the vulnerability to water deficits have profound effects on plant distribution and mortality. In this study, we compiled a leaf hydraulic trait dataset with 311 species-at-site combinations from biomes worldwide. These traits included maximum leaf hydraulic conductance (Kleaf), water potential at 50% loss of Kleaf (P50leaf), and minimum leaf water potential (Ψmin). Leaf hydraulic safety margin (HSMleaf) was calculated as the difference between Ψmin and P50leaf. Our results indicated that 70% of the studied species had a narrow HSMleaf (less than 1 MPa), which was consistent with the global pattern of stem hydraulic safety margin. There was a positive relationship between HSMleaf and aridity index (the ratio of mean annual precipitation to potential evapotranspiration), as species from humid sites tended to have larger HSMleaf. We found a significant relationship between Kleaf and P50leaf across global angiosperm woody species and within each of the different plant groups. This global analysis of leaf hydraulic traits improves our understanding of plant hydraulic response to environmental change.

The contrasting leaf functional traits between a karst forest and a nearby non-karst forest in south-west China.

Karst and non-karst forests occur in the same region in south-west China, but the soil water and mineral nutrients availability are different between the forests. Our hypothesis was that the leaves of karst trees would be better adapted to dry, nutrient-poor conditions than those of trees in a nearby non-karst forest. We compared the gas exchange, anatomical characteristics and mineral nutrient concentrations in leaves from 21 tree species in a tropical karst forest and 19 species in a nearby non-karst forest in south-west China. We found that the leaves of karst trees had higher P concentrations, photosynthetic capacity and water use efficiency, and greater adaxial and abaxial epidermis thickness than leaves of non-karst forest trees. Evergreen and deciduous trees differed more significantly in leaf functional traits in the karst forest than in the non-karst forest. The leaf palisade:spongy mesophyll thickness ratio was positively correlated with stomatal conductance and negatively correlated with photosynthetic water use efficiency in the karst forest but not in the non-karst forest. Our findings indicate that karst forest trees are more conservative in water use, whereas soil P deficiency could be a major limiting factor for the growth of non-karst forest trees.

Canopy water status and photosynthesis of tropical trees are associated with trunk sapwood hydraulic properties.

Tree trunks not only provide physical support for canopy leaves but also supply and store water for transpiration. However, the relationships between trunk hydraulic properties and canopy leaf physiology in tropical trees are not well-understood. In this study we concurrently measured morning and midday canopy leaf photosynthesis (A), stomatal conductance (gs), and leaf water potentials (ΨL) in 40 tropical trees representing 14 species at the beginning of the rainy season in Xishuangbanna, Southwest China. We also measured trunk sapwood capacitance (C), wood density, and sap flux density to assess their association with canopy leaf physiology. Among the 14 studied species, only three and four species did not show a significant midday reduction in A and gs respectively. The diurnally maximum A and gs were significantly positively related to sapwood hydraulic capacitance, maximum sap flux density (midday), and sap flux density at 11:00. Those species with lower wood density and higher C showed a lower reduction in ΨL at midday, whereas, species with high C, and large values of maximum sap flux density also showed high carbon assimilation at midday. Our results provide new insights into the close coordination between canopy physiology and trunk sapwood hydraulic properties in tropical trees.

Large branch and leaf hydraulic safety margins in subtropical evergreen broadleaved forest.

As a global biodiversity hotspot, the subtropical evergreen broadleaved forest (SEBF) in southern China is strongly influenced by the humid monsoon climate, with distinct hot-wet and cool-dry seasons. However, the hydraulic strategies of this forest are not well understood. Branch and leaf hydraulic safety margins (HSMbranch and HSMleaf, respectively), as well as seasonal changes in predawn and midday leaf water potential (Ψpd and Ψmd), stomatal conductance (Gs), leaf to sapwood area ratio (AL/AS) and turgor loss point (Ψtlp), were examined for woody species in a mature SEBF. For comparison, we compiled these traits of tropical dry forests (TDFs) and Mediterranean-type woodlands (MWs) from the literature because they experience a hot-dry season. We found that on average, SEBF showed larger HSMbranch and HSMleaf than TDF and MW. During the dry season, TDF and MW species displayed a significant decrease in Ψpd and Ψmd. However, SEBF species showed a slight decrease in Ψpd but an increase in Ψmd. Similar to TDF and MW species, Gs was substantially lower in the dry season for SEBF species, but this might be primarily because of the low atmospheric temperature (low vapor pressure deficit). On the other hand, AL/AS and Ψtlp were not significant different between seasons for any SEBF species. Most SEBF species had leaves that were more resistant to cavitation than branches. Additionally, species with stronger leaf-to-branch vulnerability segmentation tended to have smaller HSMleaf but larger HSMbranch. Our results suggest that SEBF is at low hydraulic risk under the current climate.

Leaf turgor loss point is correlated with drought tolerance and leaf carbon economics traits.

Leaf turgor loss point (πtlp) indicates the capacity of a plant to maintain cell turgor pressure during dehydration, which has been proven to be strongly predictive of the plant response to drought. In this study, we compiled a data set of πtlp for 1752 woody plant individuals belonging to 389 species from nine major woody biomes in China, along with reduced sample size of hydraulic and leaf carbon economics data. We aimed to investigate the variation of πtlp across biomes varying in water availability. We also tested two hypotheses: (i) πtlp predicts leaf hydraulic safety margins and (ii) it is correlated with leaf carbon economics traits. Our results showed that there was a positive relationship between πtlp and aridity index: biomes from humid regions had less negative values than those from arid regions. This supports the idea that πtlp may reflect drought tolerance at the scale of woody biomes. As expected, πtlp was significantly positively correlated with leaf hydraulic safety margins that varied significantly across biomes, indicating that this trait may be useful in modelling changes of forest components in response to increasing drought. Moreover, πtlp was correlated with a suite of coordinated hydraulic and economics traits; therefore, it can be used to predict the position of a given species along the 'fast-slow' whole-plant economics spectrum. This study expands our understanding of the biological significance of πtlp not only in drought tolerance, but also in the plant economics spectrum.

Different hydraulic traits of woody plants from tropical forests with contrasting soil water availability.

In southwestern China, tropical karst forests (KF) and non-karst rain forests (NKF) have different species composition and forest structure owing to contrasting soil water availability, but with a few species that occur in both forests. Plant hydraulic traits are important for understanding the species' distribution patterns in these two forest types, but related studies are rare. In this study, we investigated hydraulic conductivity, vulnerability to drought-induced cavitation and wood anatomy of 23 abundant and typical woody species from a KF and a neighboring NKF, as well as two Bauhinia liana species common to both forests. We found that the KF species tended to have higher sapwood density, smaller vessel diameter, lower specific hydraulic conductivity (ks) and leaf to sapwood area ratio, and were more resistant to cavitation than NKF species. Across the 23 species distinctly occurring in either KF or NKF, there was a significant tradeoff between hydraulic efficiency and safety, which might be an underlying mechanism for distributions of these species across the two forests. Interestingly, by possessing rather large and long vessels, the two Bauhinia liana species had extremely high ks but were also high resistance to cavitation (escaping hydraulic tradeoff). This might be partially due to their distinctly dimorphic vessels, but contribute to their wide occurrence in both forests.

Different leaf cost-benefit strategies of ferns distributed in contrasting light habitats of sub-tropical forests.

BACKGROUND AND AIMS: Ferns are abundant in sub-tropical forests in southern China, with some species being restricted to shaded understorey of natural forests, while others are widespread in disturbed, open habitats. To explain this distribution pattern, we hypothesize that ferns that occur in disturbed forests (FDF) have a different leaf cost-benefit strategy compared with ferns that occur in natural forests (FNF), with a quicker return on carbon investment in disturbed habitats compared with old-growth forests. METHODS: We chose 16 fern species from contrasting light habitats (eight FDF and eight FNF) and studied leaf functional traits, including leaf life span (LLS), specific leaf area (SLA), leaf nitrogen and phosphorus concentrations (N and P), maximum net photosynthetic rates (A), leaf construction cost (CC) and payback time (PBT), to conduct a leaf cost-benefit analysis for the two fern groups. KEY RESULTS: The two groups, FDF and FNF, did not differ significantly in SLA, leaf N and P, and CC, but FDF had significantly higher A, greater photosynthetic nitrogen- and phosphorus-use efficiencies (PNUE and PPUE), and shorter PBT and LLS compared with FNF. Further, across the 16 fern species, LLS was significantly correlated with A, PNUE, PPUE and PBT, but not with SLA and CC. CONCLUSIONS: Our results demonstrate that leaf cost-benefit analysis contributes to understanding the distribution pattern of ferns in contrasting light habitats of sub-tropical forests: FDF employing a quick-return strategy can pre-empt resources and rapidly grow in the high-resource environment of open habitats; while a slow-return strategy in FNF allows their persistence in the shaded understorey of old-growth forests.

Interspecific variation in branch and leaf traits among three Syzygium tree species from different successional tropical forests.

Plant functional traits are closely associated with plant habitats. In this study, we investigated the interspecific variations in stem and leaf hydraulics, xylem and leaf anatomy, gas-exchange rates and leaf pressure-volume relationships among three Syzygium tree species in early, mid- and late successional tropical forests. The objective was to understand the response and adaptation of congeneric species, in terms of branch and leaf functional traits, to different environments. A consistent pattern of decline with succession was evident in leaf and sapwood specific hydraulic conductivity (ks), maximum leaf hydraulic conductance (Kleaf), and photosynthetic rates for the three Syzygium species. Variations of ks and Kleaf were correlated with changes in vessel anatomy (i.e. vessel density and diameter) and leaf flux-related structure (i.e. stomatal pore index and vein density) respectively. However, specific leaf area and leaf to sapwood area ratio did not significantly differ among the three species. In addition, the mid-successional species had the lowest values of leaf water potential at full turgor and turgor loss point and 50% loss of Kleaf, but the greatest value of xylem water potential at 50% loss of ks. Our results demonstrate that leaf and branch traits associated with photosynthesis and/or hydraulic conductance, rather than those associated with drought tolerance, are the key factors underlying the response and adaptation of the three Syzygium tree species along the tropical forest succession.

Plant hydraulics and photosynthesis of 34 woody species from different successional stages of subtropical forests.

It is important to understand the ecophysiological characters of plants when exploring mechanisms underlying species substitution in the process of plant succession. In the present study, we selected 34 woody species from different stages of secondary succession in subtropical forests of southern China, and measured their hydraulic conductivity, gas exchange rates, leaf nutrients and drought-tolerance traits such as xylem resistance to cavitation, turgor loss point and carbon isotope ratio. Principal component analysis revealed that early-, mid- and late-successional species were significantly separated along axis 1, which was strongly associated with hydraulic-photosynthetic coordination. In contrast to species distributed in late-successional forest, early-successional species had the highest hydraulic conductivity, net photosynthetic rates, photosynthetic nitrogen and phosphorus use efficiencies, but had the lowest photosynthetic water-use efficiency. However, changes of the measured drought-tolerance traits of the 34 species along the succession did not demonstrate a clear trend - no significant correlations between these traits and plant successional stages were found. Moreover, the trade-off between hydraulic efficiency and safety was not identified. Taken together, our results suggested that hydraulic efficiency and photosynthetic function, rather than drought tolerance, play an important role in species distributions along plant succession in subtropical forests.

Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest.

BACKGROUND AND AIMS: The co-occurring of evergreen and deciduous angiosperm trees in Asian tropical dry forests on karst substrates suggests the existence of different water-use strategies among species. In this study it is hypothesized that the co-occurring evergreen and deciduous trees differ in stem hydraulic traits and leaf water relationships, and there will be correlated evolution in drought tolerance between leaves and stems. METHODS: A comparison was made of stem hydraulic conductivity, vulnerability curves, wood anatomy, leaf life span, leaf pressure-volume characteristics and photosynthetic capacity of six evergreen and six deciduous tree species co-occurring in a tropical dry karst forest in south-west China. The correlated evolution of leaf and stem traits was examined using both traditional and phylogenetic independent contrasts correlations. KEY RESULTS: It was found that the deciduous trees had higher stem hydraulic efficiency, greater hydraulically weighted vessel diameter (D(h)) and higher mass-based photosynthetic rate (A(m)); while the evergreen species had greater xylem-cavitation resistance, lower leaf turgor-loss point water potential (π(0)) and higher bulk modulus of elasticity. There were evolutionary correlations between leaf life span and stem hydraulic efficiency, A(m), and dry season π(0). Xylem-cavitation resistance was evolutionarily correlated with stem hydraulic efficiency, D(h), as well as dry season π(0). Both wood density and leaf density were closely correlated with leaf water-stress tolerance and A(m). CONCLUSIONS: The results reveal the clear distinctions in stem hydraulic traits and leaf water-stress tolerance between the co-occurring evergreen and deciduous angiosperm trees in an Asian dry karst forest. A novel pattern was demonstrated linking leaf longevity with stem hydraulic efficiency and leaf water-stress tolerance. The results show the correlated evolution in drought tolerance between stems and leaves.

Contrasting cost-benefit strategy between lianas and trees in a tropical seasonal rain forest in southwestern China.

Lianas are an important component of tropical forests and often abundant in open habitats, such as tree-fall gaps, forest edges, and disturbed forests. The abundance of lianas in tropical forests has been increasing as a result of global environmental change and increasing forest fragmentation. In order to understand this phenomenon in terms of leaf functional traits and to evaluate their competitive potential, we conducted a cost-benefit analysis of leaves from 18 liana species and 19 tree species in a tropical seasonal rain forest. The results revealed that lianas were scattered in a group distinct from trees along the first axis of a principal component analysis using 15 leaf ecophysiological traits, being located at the quick-return end of the leaf economics spectrum, with higher specific leaf area and photosynthetic rates (A), higher photosynthetic nitrogen (N) and phosphorus (P) use efficiencies, a lower leaf construction cost per unit leaf area (CC) and cost-benefit ratio (CC/A), and a shorter leaf life span (LLS). Trees showed the opposite trends. The results indicate that lianas can grow faster and capture resources more efficiently than trees in disturbed, open habitats. The positive relationship between LLS and CC/A revealed a trade-off between leaf construction cost and benefit over time. The 37 species analyzed had a mean foliar N/P ratio of 20, indicating that the forest was characterized by a P deficit. With an increasing atmospheric CO(2) concentration, the higher nutrient use efficiency could benefit lianas more than trees in terms of productivity, possibly also contributing to the increasing abundance of lianas in nutrient-limited tropical forests.