Differences in xylem and leaf hydraulic traits explain differences in drought tolerance among mature Amazon rainforest trees

Considerable uncertainty surrounds the impacts of anthropogenic climate change on the composition and structure of Amazon forests. Building upon results from two large‐scale ecosystem drought experiments in the eastern Brazilian Amazon that observed increases in mortality rates among some tree species but not others, in this study we investigate the physiological traits underpinning these differential demographic responses. Xylem pressure at 50% conductivity (xylem‐P₅₀), leaf turgor loss point (TLP), cellular osmotic potential (π_o), and cellular bulk modulus of elasticity (ε), all traits mechanistically linked to drought tolerance, were measured on upper canopy branches and leaves of mature trees from selected species growing at the two drought experiment sites. Each species was placed a priori into one of four plant functional type (PFT) categories: drought‐tolerant versus drought‐intolerant based on observed mortality rates, and subdivided into early‐ versus late‐successional based on wood density. We tested the hypotheses that the measured traits would be significantly different between the four PFTs and that they would be spatially conserved across the two experimental sites. Xylem‐P₅₀, TLP, and π_o, but not ε, occurred at significantly higher water potentials for the drought‐intolerant PFT compared to the drought‐tolerant PFT; however, there were no significant differences between the early‐ and late‐successional PFTs. These results suggest that these three traits are important for determining drought tolerance, and are largely independent of wood density—a trait commonly associated with successional status. Differences in these physiological traits that occurred between the drought‐tolerant and drought‐intolerant PFTs were conserved between the two research sites, even though they had different soil types and dry‐season lengths. This more detailed understanding of how xylem and leaf hydraulic traits vary between co‐occuring drought‐tolerant and drought‐intolerant tropical tree species promises to facilitate a much‐needed improvement in the representation of plant hydraulics within terrestrial ecosystem and biosphere models, which will enhance our ability to make robust predictions of how future changes in climate will affect tropical forests.     

Long-term drought effects on the thermal sensitivity of Amazon forest trees

The continued functioning of tropical forests under climate change depends on their resilience to drought and heat. However, there is little understanding of how tropical forests will respond to combinations of these stresses, and no field studies to date have explicitly evaluated whether sustained drought alters sensitivity to temperature. We measured the temperature response of net photosynthesis, foliar respiration and the maximum quantum efficiency of photosystem II (F_v/F_m) of eight hyper-dominant Amazonian tree species at the world's longest-running tropical forest drought experiment, to investigate the effect of drought on forest thermal sensitivity. Despite a 0.6°C–2°C increase in canopy air temperatures following long-term drought, no change in overall thermal sensitivity of net photosynthesis or respiration was observed. However, photosystem II tolerance to extreme-heat damage (T₅₀) was reduced from 50.0 ± 0.3°C to 48.5 ± 0.3°C under drought. Our results suggest that long-term reductions in precipitation, as projected across much of Amazonia by climate models, are unlikely to greatly alter the response of tropical forests to rising mean temperatures but may increase the risk of leaf thermal damage during heatwaves.     

Drier tropical forests are susceptible to functional changes in response to a long‐term drought

Climatic changes have profound effects on the distribution of biodiversity, but untangling the links between climatic change and ecosystem functioning is challenging, particularly in high diversity systems such as tropical forests. Tropical forests may also show different responses to a changing climate, with baseline climatic conditions potentially inducing differences in the strength and timing of responses to droughts. Trait‐based approaches provide an opportunity to link functional composition, ecosystem function and environmental changes. We demonstrate the power of such approaches by presenting a novel analysis of long‐term responses of different tropical forest to climatic changes along a rainfall gradient. We explore how key ecosystem's biogeochemical properties have shifted over time as a consequence of multi‐decadal drying. Notably, we find that drier tropical forests have increased their deciduous species abundance and generally changed more functionally than forests growing in wetter conditions, suggesting an enhanced ability to adapt ecologically to a drying environment.     

Small tropical forest trees have a greater capacity to adjust carbon metabolism to long-term drought than large canopy trees

The response of small understory trees to long-term drought is vital in determining the future composition, carbon stocks and dynamics of tropical forests. Long-term drought is, however, also likely to expose understory trees to increased light availability driven by drought-induced mortality. Relatively little is known about the potential for understory trees to adjust their physiology to both decreasing water and increasing light availability. We analysed data on maximum photosynthetic capacity (J_max, V_cmax), leaf respiration (R_leaf), leaf mass per area (LMA), leaf thickness and leaf nitrogen and phosphorus concentrations from 66 small trees across 12 common genera at the world's longest running tropical rainfall exclusion experiment and compared responses to those from 61 surviving canopy trees. Small trees increased J_max, V_cmax, R_leaf and LMA (71, 29, 32, 15% respectively) in response to the drought treatment, but leaf thickness and leaf nutrient concentrations did not change. Small trees were significantly more responsive than large canopy trees to the drought treatment, suggesting greater phenotypic plasticity and resilience to prolonged drought, although differences among taxa were observed. Our results highlight that small tropical trees have greater capacity to respond to ecosystem level changes and have the potential to regenerate resilient forests following future droughts.     

Predicting shifts in the functional composition of tropical forests under increased drought and CO2 from trade‐offs among plant hydraulic traits

Tropical forest responses are an important feedback on global change, but changes in forest composition with projected increases in CO₂ and drought are highly uncertain. Here we determine shifts in the most competitive plant hydraulic strategy (the evolutionary stable strategy or ESS) from changes in CO₂ and drought frequency and intensity. Hydraulic strategies were defined along a spectrum from drought avoidance to tolerance by physiology traits. Drought impacted competition more than CO₂, with elevated CO₂ reducing but not reversing drought‐induced shifts in the ESS towards more tolerant strategies. Trait plasticity and/or adaptation intensified these shifts by increasing the competitive ability of the drought tolerant relative to the avoidant strategies. These findings predict losses of drought avoidant evergreens from tropical forests under global change, and point to the importance of changes in precipitation during the dry season and constraints on plasticity and adaptation in xylem traits to forest responses.     

Plant functional traits explain interspecific differences in immediate cyclone damage to trees of an endangered rainforest community in north Queensland

Abstract Cyclones cause profound immediate impacts on tropical rainforest trees, including defoliation, limb loss, snapping of stems and uprooting. Some studies have shown that plant functional traits such as tree size, buttress roots and wood density are correlated with these forms of cyclone damage. On 20 March 2006, Severe Tropical Cyclone Larry crossed the north Queensland coast and proceeded inland across the Atherton Tablelands, impacting the critically endangered Mabi Type 5b rainforest. We investigated the effects of Cyclone Larry on common tree species by categorizing damage to trees as uprooted, snapped, limbs damaged (light, moderate, severe) or upright and estimating levels of defoliation. Damage was then related to functional traits including tree size, presence of buttress roots, wood density, and leaf size and strength. Levels of damage differed between species. Tree size (diameter at breast height) and the presence of buttress roots were not related to damage levels. Wood density was significantly negatively correlated to proportion of trees with snapped stems and significantly positively correlated with the proportion of trees upright with no or light limb damage. Levels of defoliation were significantly related to leaf strength (specific leaf area – SLA) and to leaf width, but not other components of leaf size (area or length) or petiole length. Species with high wood density and low SLA (e.g. Argyrodendron spp.) were found to have high cyclone resistance, the ability to resist damage, while species with low wood density and high SLA (e.g. Dendrocnide photinophylla) exhibited low resistance. However, traits related to low resistance are also those linked to rapid growth and high cyclone resilience, the ability to recover from damage, so it is unlikely that the Mabi forest will experience long‐term changes in floristic composition following Cyclone Larry.     

Functional traits determine tree growth and ecosystem productivity of a tropical montane forest: Insights from a long‐term nutrient manipulation experiment

Trait‐response effects are critical to forecast community structure and biomass production in highly diverse tropical forests. Ecological theory and few observation studies indicate that trees with acquisitive functional traits would respond more strongly to higher resource availability than those with conservative traits. We assessed how long‐term tree growth in experimental nutrient addition plots (N, P, and N + P) varied as a function of morphological traits, tree size, and species identity. We also evaluated how trait‐based responses affected stand scale biomass production considering the community structure. We found that tree growth depended on interactions between functional traits and the type or combination of nutrients added. Common species with acquisitive functional traits responded more strongly to nutrient addition, mainly to N + P. Phosphorous enhanced the growth rates of species with acquisitive and conservative traits, had mostly positive effects on common species and neutral or negative effects in rare species. Moreover, trees receiving N + P grew faster irrespective of their initial size relative to trees in control or to trees in other treatment plots. Finally, species responses were highly idiosyncratic suggesting that community processes including competition and niche dimensionality may be altered under increased resource availability. We found no statistically significant effects of nutrient additions on aboveground biomass productivity because acquisitive species had a limited potential to increase their biomass, possibly due to their generally lower wood density. In contrast, P addition increased the growth rates of species characterized by more conservative resource strategies (with higher wood density) that were poorly represented in the plant community. We provide the first long‐term experimental evidence that trait‐based responses, community structure, and community processes modulate the effects of increased nutrient availability on biomass productivity in a tropical forest.     

Plasticity in gas‐exchange physiology of mature Scots pine and European larch drive short‐ and long‐term adjustments to changes in water availability

Adjustment mechanisms of trees to changes in soil‐water availability over long periods are poorly understood, but crucial to improve estimates of forest development in a changing climate. We compared mature trees of Scots pine (Pinus sylvestris) and European larch (Larix decidua) growing along water‐permeable channels (irrigated) and under natural conditions (control) at three sites in inner‐Alpine dry valleys. At two sites, the irrigation had been stopped in the 1980s. We combined measurements of basal area increment (BAI), tree height and gas‐exchange physiology (Δ¹³C) for the period 1970–2009. At one site, the Δ¹³C of irrigated pine trees was higher than that of the control in all years, while at the other sites, it differed in pine and larch only in years with dry climatic conditions. During the first decade after the sudden change in water availability, the BAI and Δ¹³C of originally irrigated pine and larch trees decreased instantly, but subsequently reached higher levels than those of the control by 2009 (15 years afterwards). We found a high plasticity in the gas‐exchange physiology of pine and larch and site‐specific responses to changes in water availability. Our study highlights the ability of trees to adjust to new conditions, thus showing high resilience.     

Prolonged experimental drought reduces plant hydraulic conductance and transpiration and increases mortality in a piñon–juniper woodland

Plant hydraulic conductance (k_s) is a critical control on whole‐plant water use and carbon uptake and, during drought, influences whether plants survive or die. To assess long‐term physiological and hydraulic responses of mature trees to water availability, we manipulated ecosystem‐scale water availability from 2007 to 2013 in a piñon pine (Pinus edulis) and juniper (Juniperus monosperma) woodland. We examined the relationship between k_s and subsequent mortality using more than 5 years of physiological observations, and the subsequent impact of reduced hydraulic function and mortality on total woody canopy transpiration (E_C) and conductance (G_C). For both species, we observed significant reductions in plant transpiration (E) and k_s under experimentally imposed drought. Conversely, supplemental water additions increased E and k_s in both species. Interestingly, both species exhibited similar declines in k_s under the imposed drought conditions, despite their differing stomatal responses and mortality patterns during drought. Reduced whole‐plant k_s also reduced carbon assimilation in both species, as leaf‐level stomatal conductance (g_s) and net photosynthesis (A_n) declined strongly with decreasing k_s. Finally, we observed that chronically low whole‐plant k_s was associated with greater canopy dieback and mortality for both piñon and juniper and that subsequent reductions in woody canopy biomass due to mortality had a significant impact on both daily and annual canopy E_C and G_C. Our data indicate that significant reductions in k_s precede drought‐related tree mortality events in this system, and the consequence is a significant reduction in canopy gas exchange and carbon fixation. Our results suggest that reductions in productivity and woody plant cover in piñon–juniper woodlands can be expected due to reduced plant hydraulic conductance and increased mortality of both piñon pine and juniper under anticipated future conditions of more frequent and persistent regional drought in the southwestern United States.     

A 7000‐year history of changing plant trait composition in an Amazonian landscape; the role of humans and climate

Tropical forests are shifting in species and trait composition, but the main underlying causes remain unclear because of the short temporal scales of most studies. Here, we develop a novel approach by linking functional trait data with 7000 years of forest dynamics from a fossil pollen record of Lake Sauce in the Peruvian Amazon. We evaluate how climate and human disturbances affect community trait composition. We found weak relationships between environmental conditions and traits at the taxon level, but strong effects for community‐mean traits. Overall, community‐mean traits were more responsive to human disturbances than to climate change; human‐induced erosion increased the dominance of dense‐wooded, non‐zoochorous species with compound leaves, and human‐induced fire increased the dominance of tall, zoochorous taxa with large seeds and simple leaves. This information can help to enhance our understanding of forest responses to past environmental changes, and improve predictions of future changes in tropical forest composition.     

Changes in high arctic tundra plant reproduction in response to long‐term experimental warming

We provide new information on changes in tundra plant sexual reproduction in response to long‐term (12 years) experimental warming in the High Arctic. Open‐top chambers (OTCs) were used to increase growing season temperatures by 1–2 °C across a range of vascular plant communities. The warming enhanced reproductive effort and success in most species; shrubs and graminoids appeared to be more responsive than forbs. We found that the measured effects of warming on sexual reproduction were more consistently positive and to a greater degree in polar oasis compared with polar semidesert vascular plant communities. Our findings support predictions that long‐term warming in the High Arctic will likely enhance sexual reproduction in tundra plants, which could lead to an increase in plant cover. Greater abundance of vegetation has implications for primary consumers – via increased forage availability, and the global carbon budget – as a function of changes in permafrost and vegetation acting as a carbon sink. Enhanced sexual reproduction in Arctic vascular plants may lead to increased genetic variability of offspring, and consequently improved chances of survival in a changing environment. Our findings also indicate that with future warming, polar oases may play an important role as a seed source to the surrounding polar desert landscape.     

New insights on plant phenological response to temperature revealed from long‐term widespread observations in China

Constraints of temperature on spring plant phenology are closely related to plant growth, vegetation dynamics, and ecosystem carbon cycle. However, the effects of temperature on leaf onset, especially for winter chilling, are still not well understood. Using long‐term, widespread in situ phenology observations collected over China for multiple plant species, this study analyzes the quantitative response of leaf onset to temperature, and compares empirical findings with existing theories and modeling approaches, as implemented in 18 phenology algorithms. Results show that the growing degree days (GDD) required for leaf onset vary distinctly among plant species and geographical locations as well as at organizational levels (species and community), pointing to diverse adaptation strategies. Chilling durations (CHD) needed for releasing bud dormancy decline monotonously from cold to warm areas with very limited interspecies variations. Results also reveal that winter chilling is a crucial component of phenology models, and its effect is better captured with an index that accounts for the inhomogeneous effectiveness of low temperature to chilling rate than with the conventional CHD index. The impact of spring warming on leaf onset is nonlinear, better represented by a logistical function of temperature than by the linear function currently implemented in biosphere models. The optimized base temperatures for thermal accumulation and the optimal chilling temperatures are species‐dependent and average at 6.9 and 0.2°C, respectively. Overall, plants’ chilling requirement is not a constant, and more chilling generally results in less requirement of thermal accumulation for leaf onset. Our results clearly demonstrate multiple deficiencies of the parameters (e.g., base temperature) and algorithms (e.g., method for calculating GDD) in conventional phenology models to represent leaf onset. Therefore, this study not only advances our mechanistic and quantitative understanding of temperature controls on leaf onset but also provides critical information for improving existing phenology models.     

Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture

Background and Aims

Plasticity in structural and functional traits related to water balance may determine plant performance and survival in ecosystems characterized by water limitation or high levels of rainfall variability, particularly in perennial herbaceous species with long generation cycles. This paper addresses whether and the extent to which several such seasonal to long-term traits respond to changes in moisture availability.

Methods

Using a novel approach that integrates ecology, physiology and anatomy, a comparison was made of lifetime functional traits in the root xylem of a long-lived perennial herb (Potentilla diversifolia, Rosaceae) growing in dry habitats with those of nearby individuals growing where soil moisture had been supplemented for 14 years. Traditional parameters such as specific leaf area (SLA) and above-ground growth were also assessed.

Key Results

Individuals from the site receiving supplemental moisture consistently showed significant responses in all considered traits related to water balance: SLA was greater by 24 %; roots developed 19 % less starch storing tissue, an indicator for drought-stress tolerance; and vessel size distributions shifted towards wider elements that collectively conducted water 54 % more efficiently – but only during the years for which moisture was supplemented. In contrast, above-ground growth parameters showed insignificant or inconsistent responses.

Conclusions

The phenotypic changes documented represent consistent, dynamic responses to increased moisture availability that should increase plant competitive ability. The functional plasticity of xylem anatomy quantified in this study constitutes a mechanistic basis for anticipating the differential success of plant species in response to climate variability and change, particularly where water limitation occurs.     

Effects of experimental nitrogen additions on plant diversity in an old‐growth tropical forest

Response of plant biodiversity to increased availability of nitrogen (N) has been investigated in temperate and boreal forests, which are typically N‐limited, but little is known in tropical forests. We examined the effects of artificial N additions on plant diversity (species richness, density and cover) of the understory layer in an N saturated old‐growth tropical forest in southern China to test the following hypothesis: N additions decrease plant diversity in N saturated tropical forests primarily from N‐mediated changes in soil properties. Experimental additions of N were administered at the following levels from July 2003 to July 2008: no addition (Control); 50 kg N ha^?1 yr^?1 (Low‐N); 100 kg N ha^?1 yr^?1 (Medium‐N), and 150 kg N ha^?1 yr^?1 (High‐N). Results showed that no understory species exhibited positive growth response to any level of N addition during the study period. Although low‐to‐medium levels of N addition (≤100 kg N ha^?1 yr^?1) generally did not alter plant diversity through time, high levels of N addition significantly reduced species diversity. This decrease was most closely related to declines within tree seedling and fern functional groups, as well as to significant increases in soil acidity and Al mobility, and decreases in Ca availability and fine‐root biomass. This mechanism for loss of biodiversity provides sharp contrast to competition‐based mechanisms suggested in studies of understory communities in other forests. Our results suggest that high‐N additions can decrease plant diversity in tropical forests, but that this response may vary with rate of N addition.