Tropical forests are approaching critical temperature thresholds.

The critical temperature beyond which photosynthetic machinery in tropical trees begins to fail averages approximately 46.7 °C (Tcrit)1. However, it remains unclear whether leaf temperatures experienced by tropical vegetation approach this threshold or soon will under climate change. Here we found that pantropical canopy temperatures independently triangulated from individual leaf thermocouples, pyrgeometers and remote sensing (ECOSTRESS) have midday peak temperatures of approximately 34 °C during dry periods, with a long high-temperature tail that can exceed 40 °C. Leaf thermocouple data from multiple sites across the tropics suggest that even within pixels of moderate temperatures, upper canopy leaves exceed Tcrit 0.01% of the time. Furthermore, upper canopy leaf warming experiments (+2, 3 and 4 °C in Brazil, Puerto Rico and Australia, respectively) increased leaf temperatures non-linearly, with peak leaf temperatures exceeding Tcrit 1.3% of the time (11% for more than 43.5 °C, and 0.3% for more than 49.9 °C). Using an empirical model incorporating these dynamics (validated with warming experiment data), we found that tropical forests can withstand up to a 3.9 ± 0.5 °C increase in air temperatures before a potential tipping point in metabolic function, but remaining uncertainty in the plasticity and range of Tcrit in tropical trees and the effect of leaf death on tree death could drastically change this prediction. The 4.0 °C estimate is within the 'worst-case scenario' (representative concentration pathway (RCP) 8.5) of climate change predictions2 for tropical forests and therefore it is still within our power to decide (for example, by not taking the RCP 6.0 or 8.5 route) the fate of these critical realms of carbon, water and biodiversity3,4.

High exposure of global tree diversity to human pressure.

Safeguarding Earth's tree diversity is a conservation priority due to the importance of trees for biodiversity and ecosystem functions and services such as carbon sequestration. Here, we improve the foundation for effective conservation of global tree diversity by analyzing a recently developed database of tree species covering 46,752 species. We quantify range protection and anthropogenic pressures for each species and develop conservation priorities across taxonomic, phylogenetic, and functional diversity dimensions. We also assess the effectiveness of several influential proposed conservation prioritization frameworks to protect the top 17% and top 50% of tree priority areas. We find that an average of 50.2% of a tree species' range occurs in 110-km grid cells without any protected areas (PAs), with 6,377 small-range tree species fully unprotected, and that 83% of tree species experience nonnegligible human pressure across their range on average. Protecting high-priority areas for the top 17% and 50% priority thresholds would increase the average protected proportion of each tree species' range to 65.5% and 82.6%, respectively, leaving many fewer species (2,151 and 2,010) completely unprotected. The priority areas identified for trees match well to the Global 200 Ecoregions framework, revealing that priority areas for trees would in large part also optimize protection for terrestrial biodiversity overall. Based on range estimates for >46,000 tree species, our findings show that a large proportion of tree species receive limited protection by current PAs and are under substantial human pressure. Improved protection of biodiversity overall would also strongly benefit global tree diversity.

The stomatal response to vapor pressure deficit drives the apparent temperature response of photosynthesis in tropical forests.

As temperature rises, net carbon uptake in tropical forests decreases, but the underlying mechanisms are not well understood. High temperatures can limit photosynthesis directly, for example by reducing biochemical capacity, or indirectly through rising vapor pressure deficit (VPD) causing stomatal closure. To explore the independent effects of temperature and VPD on photosynthesis we analyzed photosynthesis data from the upper canopies of two tropical forests in Panama with Generalized Additive Models. Stomatal conductance and photosynthesis consistently decreased with increasing VPD, and statistically accounting for VPD increased the optimum temperature of photosynthesis (Topt) of trees from a VPD-confounded apparent Topt of c. 30-31°C to a VPD-independent Topt of c. 33-36°C, while for lianas no VPD-independent Topt was reached within the measured temperature range. Trees and lianas exhibited similar temperature and VPD responses in both forests, despite 1500 mm difference in mean annual rainfall. Over ecologically relevant temperature ranges, photosynthesis in tropical forests is largely limited by indirect effects of warming, through changes in VPD, not by direct warming effects of photosynthetic biochemistry. Failing to account for VPD when determining Topt misattributes the underlying causal mechanism and thereby hinders the advancement of mechanistic understanding of global warming effects on tropical forest carbon dynamics.

A medida que aumenta la temperatura, disminuye la absorción neta de carbono en los bosques tropicales, sin embargo, aún no se conocen bien los mecanismos que la subyacen. Las altas temperaturas pueden limitar la fotosíntesis directamente, por ejemplo, reduciendo la eficiencia de los procesos bioquímicos, pero también de forma indirecta a través del aumento del déficit de presión de vapor (DPV) que resulta en el cierre estomático. Para explorar los efectos independientes de la temperatura y el DPV en la fotosíntesis, analizamos datos de la absorción neta de carbono del dosel de dos bosques tropicales en Panamá utilizando modelos aditivos generalizados. La conductancia estomática y la fotosíntesis disminuyó consistentemente con el aumento de DPV, y considerando el DPV en modelas estadísticas, la temperatura óptima de la fotosíntesis (Topt) aumentó, de un Topt aparente influida por la DVP de c. 30­31°C a un Topt independiente del DPV de c. 33­36°C. Los árboles y las lianas mostraron respuestas similares a la temperatura y a la DVP en ambos bosques, a pesar de la diferencia de 1500 mm en la precipitación media anual. La fotosíntesis en los bosques tropicales está limitada en gran medida por los efectos indirectos del aumento de la temperatura, a través de cambios en el DPV y no por los efectos directos en los procesos bioquímicos. Si no se tiene en cuenta el DPV al determinar el Topt, se atribuye erróneamente el mecanismo causal subyacente y, por lo tanto, se obstaculiza el avance en la comprensión de los efectos del calentamiento global en la dinámica del carbono.

Plant water use theory should incorporate hypotheses about extreme environments, population ecology, and community ecology.

Plant water use theory has largely been developed within a plant-performance paradigm that conceptualizes water use in terms of value for carbon gain and that sits within a neoclassical economic framework. This theory works very well in many contexts but does not consider other values of water to plants that could impact their fitness. Here, we survey a range of alternative hypotheses for drivers of water use and stomatal regulation. These hypotheses are organized around relevance to extreme environments, population ecology, and community ecology. Most of these hypotheses are not yet empirically tested and some are controversial (e.g. requiring more agency and behavior than is commonly believed possible for plants). Some hypotheses, especially those focused around using water to avoid thermal stress, using water to promote reproduction instead of growth, and using water to hoard it, may be useful to incorporate into theory or to implement in Earth System Models.

Thermal sensitivity across forest vertical profiles: patterns, mechanisms, and ecological implications.

Rising temperatures are influencing forests on many scales, with potentially strong variation vertically across forest strata. Using published research and new analyses, we evaluate how microclimate and leaf temperatures, traits, and gas exchange vary vertically in forests, shaping tree, and ecosystem ecology. In closed-canopy forests, upper canopy leaves are exposed to the highest solar radiation and evaporative demand, which can elevate leaf temperature (Tleaf ), particularly when transpirational cooling is curtailed by limited stomatal conductance. However, foliar traits also vary across height or light gradients, partially mitigating and protecting against the elevation of upper canopy Tleaf . Leaf metabolism generally increases with height across the vertical gradient, yet differences in thermal sensitivity across the gradient appear modest. Scaling from leaves to trees, canopy trees have higher absolute metabolic capacity and growth, yet are more vulnerable to drought and damaging Tleaf than their smaller counterparts, particularly under climate change. By contrast, understory trees experience fewer extreme high Tleaf 's but have fewer cooling mechanisms and thus may be strongly impacted by warming under some conditions, particularly when exposed to a harsher microenvironment through canopy disturbance. As the climate changes, integrating the patterns and mechanisms reviewed here into models will be critical to forecasting forest-climate feedback.

Thermal optimum of photosynthesis is controlled by stomatal conductance and does not acclimate across an urban thermal gradient in six subtropical tree species.

Modelling the response of plants to climate change is limited by our incomplete understanding of the component processes of photosynthesis and their temperature responses within and among species. For ≥20 individuals, each of six common subtropical tree species occurring across steep urban thermal gradients in Miami, Florida, USA, we determined rates of net photosynthesis (Anet ), maximum RuBP carboxylation, maximum RuBP regeneration and stomatal conductance, and modelled the optimum temperature (Topt ) and process rate of each parameter to address two questions: (1) Do the Topt of Anet (ToptA ) and the maximum Anet (Aopt ) of subtropical trees reflect acclimation to elevated growth temperatures? And (2) What limits Anet in subtropical trees? Against expectations, we did not find significant acclimation of ToptA , Aopt  or the Topt of any of the underlying photosynthetic parameters to growth temperature in any of the focal species. Model selection for the single best predictor of Anet both across leaf temperatures and at ToptA revealed that the Anet of most trees was best predicted by stomatal conductance. Our findings are in accord with those of previous studies, especially in the tropics, that have identified stomatal conductance to be the most important factor limiting Anet , rather than biochemical thermal responses.

The acquisitive-conservative axis of leaf trait variation emerges even in homogeneous environments.

BACKGROUND AND AIMS: The acquisitive-conservative axis of plant ecological strategies results in a pattern of leaf trait covariation that captures the balance between leaf construction costs and plant growth potential. Studies evaluating trait covariation within species are scarcer, and have mostly dealt with variation in response to environmental gradients. Little work has been published on intraspecific patterns of leaf trait covariation in the absence of strong environmental variation. METHODS: We analysed covariation of four leaf functional traits [specific leaf area (SLA) leaf dry matter content (LDMC), force to tear (Ft) and leaf nitrogen content (Nm)] in six Poaceae and four Fabaceae species common in the dry Chaco forest of Central Argentina, growing in the field and in a common garden. We compared intraspecific covariation patterns (slopes, correlation and effect size) of leaf functional traits with global interspecific covariation patterns. Additionally, we checked for possible climatic and edaphic factors that could affect the intraspecific covariation pattern. KEY RESULTS: We found negative correlations for the LDMC-SLA, Ft-SLA, LDMC-Nm and Ft-Nm trait pairs. This intraspecific covariation pattern found both in the field and in the common garden and not explained by climatic or edaphic variation in the field follows the expected acquisitive-conservative axis. At the same time, we found quantitative differences in slopes among different species, and between these intraspecific patterns and the interspecific ones. Many of these differences seem to be idiosyncratic, but some appear consistent among species (e.g. all the intraspecific LDMC-SLA and LDMC-Nm slopes tend to be shallower than the global pattern). CONCLUSIONS: Our study indicates that the acquisitive-conservative leaf functional trait covariation pattern occurs at the intraspecific level even in the absence of relevant environmental variation in the field. This suggests a high degree of variation-covariation in leaf functional traits not driven by environmental variables.

Large differences in leaf cuticle conductance and its temperature response among 24 tropical tree species from across a rainfall gradient.

More frequent droughts and rising temperatures pose serious threats to tropical forests. When stomata are closed under dry and hot conditions, plants lose water through leaf cuticles, but little is known about cuticle conductance (gmin ) of tropical trees, how it varies among species and environments, and how it is affected by temperature. We determined gmin in relation to temperature for 24 tropical tree species across a steep rainfall gradient in Panama, by recording leaf drying curves at different temperatures in the laboratory. In contrast with our hypotheses, gmin did not differ systematically across the rainfall gradient; species differences did not reflect phylogenetic patterns; and in most species gmin did not significantly increase between 25 and 50°C. gmin was higher in deciduous than in evergreen species, in species with leaf trichomes than in species without, in sun leaves than in shade leaves, and tended to decrease with increasing leaf mass per area across species. There was no relationship between stomatal and cuticle conductance. Large species differences in gmin and its temperature response suggest that more frequent hot droughts may lead to differential survival among tropical tree species, regardless of species' position on the rainfall gradient.

Photosynthetic plasticity of a tropical tree species, Tabebuia rosea, in response to elevated temperature and [CO2 ].

Atmospheric and climate change will expose tropical forests to conditions they have not experienced in millions of years. To better understand the consequences of this change, we studied photosynthetic acclimation of the neotropical tree species Tabebuia rosea to combined 4°C warming and twice-ambient (800 ppm) CO2 . We measured temperature responses of the maximum rates of ribulose 1,5-bisphosphate carboxylation (VCMax ), photosynthetic electron transport (JMax ), net photosynthesis (PNet ), and stomatal conductance (gs ), and fitted the data using a probabilistic Bayesian approach. To evaluate short-term acclimation plants were then switched between treatment and control conditions and re-measured after 1-2 weeks. Consistent with acclimation, the optimum temperatures (TOpt ) for VCMax , JMax and PNet were 1-5°C higher in treatment than in control plants, while photosynthetic capacity (VCMax , JMax , and PNet at TOpt ) was 8-25% lower. Likewise, moving control plants to treatment conditions moderately increased temperature optima and decreased photosynthetic capacity. Stomatal density and sensitivity to leaf-to-air vapour pressure deficit were not affected by growth conditions, and treatment plants did not exhibit stronger stomatal limitations. Collectively, these results illustrate the strong photosynthetic plasticity of this tropical tree species as even fully developed leaves of saplings transferred to extreme conditions partially acclimated.

Leaf heat tolerance of 147 tropical forest species varies with elevation and leaf functional traits, but not with phylogeny.

Exceeding thermal thresholds causes irreversible damage and ultimately loss of leaves. The lowland tropics are among the warmest forested biomes, but little is known about heat tolerance of tropical forest plants. We surveyed leaf heat tolerance of sun-exposed leaves from 147 tropical lowland and pre-montane forest species by determining the temperatures at which potential photosystem II efficiency based on chlorophyll a fluorescence started to decrease (TCrit ) and had decreased by 50% (T50 ). TCrit averaged 46.7°C (5th-95th percentile: 43.5°C-49.7°C) and T50 averaged 49.9°C (47.8°C-52.5°C). Heat tolerance partially adjusted to site temperature; TCrit and T50 decreased with elevation by 0.40°C and 0.26°C per 100 m, respectively, while mean annual temperature decreased by 0.63°C per 100 m. The phylogenetic signal in heat tolerance was weak, suggesting that heat tolerance is more strongly controlled by environment than by evolutionary legacies. TCrit increased with the estimated thermal time constant of the leaves, indicating that species with thermally buffered leaves maintain higher heat tolerance. Among lowland species, T50 increased with leaf mass per area, suggesting that in species with structurally more costly leaves the risk of leaf loss during hot spells is reduced. These results provide insight in variation in heat tolerance at local and regional scales.

Photosynthetic quantum efficiency in south-eastern Amazonian trees may be already affected by climate change.

Tropical forests are experiencing unprecedented high-temperature conditions due to climate change that could limit their photosynthetic functions. We studied the high-temperature sensitivity of photosynthesis in a rainforest site in southern Amazonia, where some of the highest temperatures and most rapid warming in the Tropics have been recorded. The quantum yield (Fv /Fm ) of photosystem II was measured in seven dominant tree species using leaf discs exposed to varying levels of heat stress. T50 was calculated as the temperature at which Fv /Fm was half the maximum value. T5 is defined as the breakpoint temperature, at which Fv /Fm decline was initiated. Leaf thermotolerance in the rapidly warming southern Amazonia was the highest recorded for forest tree species globally. T50 and T5 varied between species, with one mid-storey species, Amaioua guianensis, exhibiting particularly high T50 and T5 values. While the T50 values of the species sampled were several degrees above the maximum air temperatures experienced in southern Amazonia, the T5 values of several species are now exceeded under present-day maximum air temperatures.

Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale.

The temperature response of photosynthesis is one of the key factors determining predicted responses to warming in global vegetation models (GVMs). The response may vary geographically, owing to genetic adaptation to climate, and temporally, as a result of acclimation to changes in ambient temperature. Our goal was to develop a robust quantitative global model representing acclimation and adaptation of photosynthetic temperature responses. We quantified and modelled key mechanisms responsible for photosynthetic temperature acclimation and adaptation using a global dataset of photosynthetic CO2 response curves, including data from 141 C3 species from tropical rainforest to Arctic tundra. We separated temperature acclimation and adaptation processes by considering seasonal and common-garden datasets, respectively. The observed global variation in the temperature optimum of photosynthesis was primarily explained by biochemical limitations to photosynthesis, rather than stomatal conductance or respiration. We found acclimation to growth temperature to be a stronger driver of this variation than adaptation to temperature at climate of origin. We developed a summary model to represent photosynthetic temperature responses and showed that it predicted the observed global variation in optimal temperatures with high accuracy. This novel algorithm should enable improved prediction of the function of global ecosystems in a warming climate.

Photosynthetic heat tolerance of shade and sun leaves of three tropical tree species.

Previous studies of heat tolerance of tropical trees have focused on canopy leaves exposed to full sunlight and high temperatures. However, in lowland tropical forests with leaf area indices of 5-6, the vast majority of leaves experience varying degrees of shade and a reduced heat load compared to sun leaves. Here we tested whether heat tolerance is lower in shade than in sun leaves. For three tropical tree species, Calophyllum inophyllum, Inga spectabilis, and Ormosia macrocalyx, disks of fully developed shade and sun leaves were subjected to 15-min heat treatments, followed by measurement of chlorophyll a fluorescence after 48 h of recovery. In two of the three species, the temperature causing a 50% decrease of the fluorescence ratio Fv/Fm (T50) was significantly lower (by ~ 1.0 °C) in shade than in sun leaves, indicating a moderately decreased heat tolerance of shade leaves. In shade leaves of these two species, the rise in initial fluorescence, F0, also occurred at lower temperatures. In the third species, there was no shade-sun difference in T50. In situ measurements of photosynthetic CO2 assimilation showed that the optimum temperature for photosynthesis tended to be lower in shade leaves, although differences were not significant. At supra-optimal temperatures, photosynthesis was largely constrained by stomatal conductance, and the high-temperature CO2 compensation point, TMax, occurred at considerably lower temperatures than T50. Our study demonstrates that the temperature response of shade leaves of tropical trees differs only marginally from that of sun leaves, both in terms of heat tolerance and photosynthetic performance.

The capacity to emit isoprene differentiates the photosynthetic temperature responses of tropical plant species.

Experimental research shows that isoprene emission by plants can improve photosynthetic performance at high temperatures. But whether species that emit isoprene have higher thermal limits than non-emitting species remains largely untested. Tropical plants are adapted to narrow temperature ranges and global warming could result in significant ecosystem restructuring due to small variations in species' thermal tolerances. We compared photosynthetic temperature responses of 26 co-occurring tropical tree and liana species to test whether isoprene-emitting species are more tolerant to high temperatures. We classified species as isoprene emitters versus non-emitters based on published datasets. Maximum temperatures for net photosynthesis were ~1.8°C higher for isoprene-emitting species than for non-emitters, and thermal response curves were 24% wider; differences in optimum temperatures (Topt ) or photosynthetic rates at Topt were not significant. Modelling the carbon cost of isoprene emission, we show that even strong emission rates cause little reduction in the net carbon assimilation advantage over non-emitters at supraoptimal temperatures. Isoprene emissions may alleviate biochemical limitations, which together with stomatal conductance, co-limit photosynthesis above Topt . Our findings provide evidence that isoprene emission may be an adaptation to warmer thermal niches, and that emitting species may fare better under global warming than co-occurring non-emitting species.

In situ temperature response of photosynthesis of 42 tree and liana species in the canopy of two Panamanian lowland tropical forests with contrasting rainfall regimes.

Tropical forests contribute significantly to the global carbon cycle, but little is known about the temperature response of photosynthetic carbon uptake in tropical species, and how this varies within and across forests. We determined in situ photosynthetic temperature-response curves for upper canopy leaves of 42 tree and liana species from two tropical forests in Panama with contrasting rainfall regimes. On the basis of seedling studies, we hypothesized that species with high photosynthetic capacity - light-demanding, fast-growing species - would have a higher temperature optimum of photosynthesis (TOpt ) than species with low photosynthetic capacity - shade-tolerant, slow-growing species - and that, therefore, TOpt would scale with the position of a species on the slow-fast continuum of plant functional traits. TOpt was remarkably similar across species, regardless of their photosynthetic capacity and other plant functional traits. Community-average TOpt was almost identical to mean maximum daytime temperature, which was higher in the dry forest. Photosynthesis above TOpt appeared to be more strongly limited by stomatal conductance in the dry forest than in the wet forest. The observation that all species in a community shared similar TOpt values suggests that photosynthetic performance is optimized under current temperature regimes. These results should facilitate the scaling up of photosynthesis in relation to temperature from leaf to stand level in species-rich tropical forests.

In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species.

Net photosynthetic carbon uptake of Panamanian lowland tropical forest species is typically optimal at 30-32 °C. The processes responsible for the decrease in photosynthesis at higher temperatures are not fully understood for tropical trees. We determined temperature responses of maximum rates of RuBP-carboxylation (VCMax ) and RuBP-regeneration (JMax ), stomatal conductance (Gs ), and respiration in the light (RLight ) in situ for 4 lowland tropical tree species in Panama. Gs had the lowest temperature optimum (TOpt ), similar to that of net photosynthesis, and photosynthesis became increasingly limited by stomatal conductance as temperature increased. JMax peaked at 34-37 °C and VCMax ~2 °C above that, except in the late-successional species Calophyllum longifolium, in which both peaked at ~33 °C. RLight significantly increased with increasing temperature, but simulations with a photosynthesis model indicated that this had only a small effect on net photosynthesis. We found no evidence for Rubisco-activase limitation of photosynthesis. TOpt of VCMax and JMax fell within the observed in situ leaf temperature range, but our study nonetheless suggests that net photosynthesis of tropical trees is more strongly influenced by the indirect effects of high temperature-for example, through elevated vapour pressure deficit and resulting decreases in stomatal conductance-than by direct temperature effects on photosynthetic biochemistry and respiration.

Photosynthetic acclimation to warming in tropical forest tree seedlings.

Tropical forests have a mitigating effect on man-made climate change by acting as a carbon sink. For that effect to continue, tropical trees will have to acclimate to rising temperatures, but it is currently unknown whether they have this capacity. We grew seedlings of three tropical tree species over a range of temperature regimes (TGrowth = 25, 30, 35 °C) and measured the temperature response of photosynthetic CO2 uptake. All species showed signs of acclimation: the temperature-response curves shifted, such that the temperature at which photosynthesis peaked (TOpt) increased with increasing TGrowth. However, although TOpt shifted, it did not reach TGrowth at high temperature, and this difference between TOpt and TGrowth increased with increasing TGrowth, indicating that plants were operating at supra-optimal temperatures for photosynthesis when grown at high temperatures. The high-temperature CO2 compensation point did not increase with TGrowth. Hence, temperature-response curves narrowed with increasing TGrowth. TOpt correlated with the ratio of the RuBP regeneration capacity over the RuBP carboxylation capacity, suggesting that at high TGrowth photosynthetic electron transport rate associated with RuBP regeneration had greater control over net photosynthesis. The results show that although photosynthesis of tropical trees can acclimate to moderate warming, carbon gain decreases with more severe warming.

The effects of CO2 and nutrient fertilisation on the growth and temperature response of the mangrove Avicennia germinans.

In order to understand plant responses to both the widespread phenomenon of increased nutrient inputs to coastal zones and the concurrent rise in atmospheric CO2 concentrations, CO2-nutrient interactions need to be considered. In addition to its potential stimulating effect on photosynthesis and growth, elevated CO2 affects the temperature response of photosynthesis. The scarcity of experiments testing how elevated CO2 affects the temperature response of tropical trees hinders our ability to model future primary productivity. In a glasshouse study, we examined the effects of elevated CO2 (800 ppm) and nutrient availability on seedlings of the widespread mangrove Avicennia germinans. We assessed photosynthetic performance, the temperature response of photosynthesis, seedling growth and biomass allocation. We found large synergistic gains in both growth (42 %) and photosynthesis (115 %) when seedlings grown under elevated CO2 were supplied with elevated nutrient concentrations relative to their ambient growing conditions. Growth was significantly enhanced under elevated CO2 only under high-nutrient conditions, mainly in above-ground tissues. Under low-nutrient conditions and elevated CO2, root volume was more than double that of seedlings grown under ambient CO2 levels. Elevated CO2 significantly increased the temperature optimum for photosynthesis by ca. 4 °C. Rising CO2 concentrations are likely to have a significant positive effect on the growth rate of A. germinans over the next century, especially in areas where nutrient availability is high.