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Among‐sites and ‐species variation in (a) critical temperature (Tcrit, °C) and the temperatures at which the Fv/Fm is reduced by (b) 20% (T20, °C) and (c) 50% (T50, °C) compared to nonheat stressed conditions. Hmo, Harungana montana (white); Sgu, Syzygium guineense (cyan); Eex, Entandrophragma exselsum (green). Data are shown as mean ± SE of the fitted temperature values. Upper case letters indicate significant among‐sites differences within each species (P = 0.05). Lower case letters indicate significant among‐species differences within each site (P = 0.05). The statistical comparisons among the groups were made using Welch's t‐tests and are detailed in Supporting Information Tables S3–S5.
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Warming climate increases the risk for harmful leaf temperatures in terrestrial plants, causing heat stress and loss of productivity. The heat sensitivity may be particularly high in equatorial tropical tree species adapted to a thermally stable climate.
Thermal thresholds of the photosynthetic system of sun‐exposed leaves were investigated in thre...
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The global demand for tropical hardwood continues to rise. However, exacerbated by a warming climate, high temperatures, and drought conditions during the dry season in many tropical regions is likely a contributing factor in the low survival rates of some planted hardwood tree seedlings grown under natural field conditions without watering. Here,...
Citations
... Since thermally induced harmful effects on plant fitness are expected to become more frequent in the current scenario of global warming, there has been a recent upsurge of interest in the possible means whereby plants could buffer, alleviate, and/or tolerate the effects of rising ambient temperatures and increasing frequency of heatwaves (Lorenzo et al., 2021;Perkins-Kirkpatrick & Lewis, 2020). Most of these studies have focused on the plants' vegetative parts and, more specifically, have addressed the possibility that the long-known ability of leaves to cool themselves to temperatures lower than the ambient (Drake et al., 1970;Ehrler, 1973;Linacre, 1964Linacre, , 1967Pearcy et al., 1972;Smith, 1978;Upchurch & Mahan, 1988) could provide a community-wide thermoregulatory mechanism allowing a "thermal escape" to leaves in the face of rising temperatures (Cook et al., 2021;Manzi et al., 2024;Michaletz et al., 2016;Posch et al., 2024;Still et al., 2022;Tarvainen et al., 2022). Few ecological studies, however, have explicitly examined to date how wild plants can cope with exposure of reproductive structures to high temperatures, despite the fact that the reproductive phase seems more sensitive to elevated temperatures than the vegetative one (Chaturvedi et al., 2021;Lohani et al., 2020;Tushabe & Rosbakh, 2024). ...
Flower exposure to high temperature reduces the production, viability, and performance of pollen, ovules, and seeds, which in turn impairs individual fecundity and risks the survival of populations. Autonomous floral cooling could alleviate the effects of flower exposure to harmful temperatures, yet investigations on thermal ecology of flowers in hot environments are needed to evaluate the reality, magnitude, and ecological significance of thermoregulatory cooling. This paper reports a study on the thermal ecology of the flower heads (=capitula) of 15 species of summer‐blooming Asteraceae, tribe Cardueae, from hot‐dry habitats in the southern Iberian Peninsula. Temperature inside (Tin) and outside (Tout) capitula were assessed under natural field conditions using two complementary sampling and measurement procedures, which provided information on the relationships between the two temperatures at the levels of individual capitula (“continuous recording”) and local plant populations (“instantaneous measurements”). Baselines for the Tin–Tout relationship in the absence of physiological activity were obtained by exposing dehydrated capitula to variable ambient temperatures in the field. To assess whether the co‐flowering capitula of summer‐blooming Asteraceae defined collectively a distinct thermal layer, the vertical distribution of capitula relative to the ground was quantified. Bees visiting capitula were watched and temperature of the air beside the visited capitulum was measured. Results were remarkably similar for all plant species. The capitula experienced high ambient temperatures during long periods, yet their interior was cooler than the air most of the time, with temperature differentials (ΔT = Tin − Tout) often approaching, and sometimes exceeding −10°C. The relationship between Tin and Tout was best described by a composite of one steep and one shallow linear relationship separated by a breakpoint (Ψ, interspecific range = 25–35°C). Capitula were only weakly thermoregulated when Tout < Ψ, but switched to closely thermoregulated cooling when Tout > Ψ. Narrow vertical distributions of capitula above the ground and similar cooling responses by all species resulted in a “refrigerated floral layer” where most bees foraged at Tout > Ψ and presumably visited cooled capitula. Thermoregulatory refrigeration of capitula (“thermal engineering”) can benefit not only plant reproduction by reducing pollen and ovule exposure to high temperatures during the summer but also the populations of bee pollinators and other floricolous insects.
... Large species variability across experimentally applied temperature treatments in transplant studies has been observed, with effects ranging from positive to negative on survival, photosynthesis, growth and leaf functional traits 19,41,48,49 supporting results obtained in this study. Such species differences may be related to different growth strategies 50 . For example, large variation in sensitivity to warming was found in a transplant experiment with Afromontane forest tree species in Rwanda 19 . ...
In tropical montane forests, the Earth’s largest biodiversity hotspots, there is increasing evidence that climate warming is resulting in montane species being displaced by their lowland counterparts. However, the drivers of these changes are poorly understood. Across a large elevation gradient in the Colombian Andes, we established three experimental plantations of 15 dominant tree species including both naturally occurring montane and lowland species and measured their survival and growth. Here we show that 55% of the studied montane species maintained growth at their survival’s hottest temperature with the remaining 45% being intolerant to such levels of warming, declining their growth, while lowland species benefited strongly from the warmest temperatures. Our findings suggest that the direct negative effects of warming and increased competition of montane species with lowland species are promoting increased homogeneity in community composition, resulting in reduced biodiversity.
... Thus, exposure time statistics are difficult to determine. In contrast to the sparseness of suitable leaf temperature records, data of measures of thermal limits to photosystems (T 50 ) and more generally photosynthesis of tropical forest trees are becoming increasingly available (Sastry and Barua 2017;Sastry, Guha, and Barua 2018;Perez and Feeley 2020;Slot et al. 2021;Araújo et al. 2021;Kitudom et al. 2022;Tarvainen et al. 2022;Tiwari et al. 2021;Kullberg et al. 2024). Several studies have focused on both thermotolerance and "thermal safety margins," the difference between leaf temperatures and measures of thermal limits (like T 50 ), in the tropics (e.g., Araújo et al. 2021;Doughty and Goulden 2008;Doughty et al. 2023;Kitudom et al. 2022); however, they have generally not considered the role of exposure time above temperature thresholds to assess leaf vulnerability to heat. ...
Increasing temperatures in the tropics will reduce performance of trees and agroforestry species and may lead to lasting damage and leaf death. One criterion to determine future forest resilience is to evaluate damage caused by temperature on Photosystem‐II (PSII), a particularly sensitive component of photosynthesis. The temperature at which 50% of PSII function is lost ( T 50 ) is a widely used measure of irreversible damage to leaves. To assess vulnerability to high temperatures, studies have measured T 50 or leaf temperatures, but rarely both. Further, because extant leaf temperature records are short, duration of exposure above thresholds like T 50 has not been considered. Finally, these studies do not directly assess the effect of threshold exceedance on leaves. To understand how often, and how long, leaf temperatures exceed critical thresholds, we measured leaf temperatures of forest and agroforestry species in a tropical forest in the Western Ghats of India where air temperatures are high. We quantified species‐specific physiological thresholds and assessed leaf damage after high‐temperature exposure. We found that leaf temperatures already exceed T 50 . However, continuous exposure durations above critical thresholds are very skewed with most events lasting for much less than 30 min. As T 50 was measured after a 30‐min exposure, our results suggest that threshold exceedances and exposure durations for lasting damage are currently not reached and will rarely be reached if maximum air temperatures increase by 4°C. Consistent with this, we found only minor indications of heat damage in the forest species. However, there were indications of heat‐induced reduction in PSII function and damage in the agroforestry leaves which have lower T 50 . Our findings suggest that, for forest species, while high‐temperature thresholds may be surpassed, durations of exposure above thresholds remain short, and therefore, are unlikely to lead to irreversible damage and leaf death, even under 4°C warming.
... Conversely, A3 and A5 exhibited significant recovery in A n and Φ PSII after irrigation. Photosystem II is considered one of the most heat-sensitive components of the photosynthetic apparatus (Maxwell and Johnson 2000;Murchie and Lawson 2013;Teskey et al. 2015;Yamamoto 2016;Niinemets 2018;Tarvainen et al. 2022), and recovery in these accessions suggests a limited impact on J as well, which can be irreversibly reduced by heat stress (Sharkey 2005;Schrader et al. 2004;Hüve et al. 2011). A3 and A5 also showed higher g s during pre-HW conditions ( Figure 2B,F) in line with findings for their inherent differences in photosynthesis (Momayyezi et al. 2022). ...
Heat waves (HWs) pose a significant threat to California agriculture, with potential adverse effects on crop photosynthetic capacity, quality and yield, all of which contribute to significant economic loss. Lack of heat‐resilient cultivars puts perennial crop production under severe threat due to increasing HW frequency, duration and intensity. Currently, available walnut cultivars are highly sensitive to abiotic stress, and germplasm collections provide potential solutions via genotypes native to varied climates. We screened nine English walnut accessions ( Juglans regia ) for physiological heat stress resilience and recovery in the USDA‐ARS National Clonal Germplasm over 2‐years, and identified accessions with superior resilience to heat stress. Heat stress impacted photosynthetic capacity in most accessions, as evidenced by reductions in net ( A n ) and maximum ( A max ) assimilation rates, quantum efficiency of PSII, and changes in stomatal conductance ( g s ). However, two accessions exhibited either higher or complete recovery post‐irrigation. This aligns with the established practice of using irrigation to mitigate heat stress, as it improved recovery for several accessions, with A3 and A5 demonstrating the most resilience. One of these two superior accessions is native to one of the hottest and driest habitats of all studied accessions. These same accessions exhibited the highest A n under non‐stressed conditions and at higher temperatures of 35° to 45°C. Higher performance for A3 and A5 under HWs was associated with greater carboxylation rates, electron transport rates, and A max . All accessions suffered significant declines in photosynthetic performance at 45°C, which were the ambient leaf temperatures approached during record‐setting heat waves in California during September 2022.
... The energy balance theory, useful for modeling leaf temperatures, incorporates environmental factors such as solar radiation, wind, relative humidity, and morphological and physiological leaf traits such as g s , E and LW (Michaletz et al. 2015), enabling the understanding of how plants adjust and compensate their traits to regulate internal leaf temperature depending on the environment (Vårhammar et al. 2015). For instance, studies have shown that reducing leaf size and increasing E improve T (Vårhammar et al. 2015, Tarvainen et al. 2022. Investigating the T between individuals growing in different urban environments, especially within UHIs, offers valuable insights into the ability of a species to avoid extreme leaf temperatures. ...
... Photosynthesis is especially sensitive to temperature variation, peaking at a species-specific optimum before declining at higher temperatures (Vårhammar et al. 2015, Tarvainen et al. 2022. The optimal temperature for photosynthesis (T opt ) aligns with the local daytime temperatures, suggesting acclimation or local adaptation (Vårhammar et al. 2015). ...
... To analyze if there are signs of physiological acclimation in the photosynthetic thermal optimum (T opt ), we used Welch's t-test to evaluate the effect of urban environments on variation in T opt . This analysis calculates the degree of overlap of the SE for T opt and optimal carbon assimilation (P opt ) (Tarvainen et al. 2022). This test is appropriate for situations where the variances of the two groups are different, and the sample size between groups is unequal (case of CEOC). ...
Urban Heat Islands (UHI) are a common phenomenon in metropolitan areas worldwide where the air temperature is significantly higher in urban areas than in surrounding suburban, rural or natural areas. Mitigation strategies to counteract UHI effects include increasing tree cover and green spaces to reduce heat. The successful application of these approaches necessitates a deep understanding of the thermal tolerances in urban trees and their susceptibility to elevated urban temperatures. We evaluated how the photosynthetic thermal optimum (Topt), photosynthetic heat tolerance (T50), and key leaf thermoregulatory morphological traits (leaf area, specific leaf area, leaf width, thickness and LDMC) differ between conspecific trees growing in ‘hot [UHI]’ vs. ‘cool’ parts of Montreal, Canada (with a difference of 3.4 °C in air temperature), to assess the ability of seven common tree species to acclimation to higher temperatures. We hypothesized that individuals with hotter growing temperatures would exhibit higher Topt and T50, as well as leaf thermoregulatory morphological traits aligned with conservative strategies (e.g., reduced leaf area and increased leaf mass) compared to their counterparts in the cooler parts of the city. Contrary to our a priori hypotheses, leaf area increased with growing temperatures and only four of the seven species had higher T50 and only three had higher Topt values in the hotter area. These results suggest that many tree species cannot acclimate to elevated temperatures and that the important services they provide, such as carbon capture, can be negatively affected by high temperatures caused by climate change and/or the UHI effect. The ability vs inability of tree species to acclimate to high temperatures should be considered when implementing long term tree planting programs in urban areas.
... These observations challenge the notion that classic, time-consuming visible inspection of leaves can be substituted by measuring F v /F m (24 h). Even though F v /F m decreases determined shortly after heat events are a useful measure of 'leaf photosynthetic heat tolerance' and may be associated with decreases in net CO 2 uptake (Tarvainen et al. 2022), they are not necessarily a measure of thermotolerance sensu strictu, that is, the upper temperature threshold above which irreversible damage occurs. ...
Tropical rainforests are hot and may be particularly sensitive to ongoing anthropogenic global warming. This has led to increased interest in the thermotolerance of tropical trees.
Thermotolerance of leaves of two tropical tree species, Terminalia catappa and Coccoloba uvifera, was determined by exposing leaf samples to 15‐min heat treatments, followed by measurements of potential photosystem II quantum yield (dark‐adapted value of variable/maximum chlorophyll a fluorescence, F v / F m ) after 24 h and 14 days, and visible damage (necrosis) after 14 days.
T 50 (24 h), the temperature at which F v / F m declined by 50% 24 h after heat treatments, was associated with only ~10% leaf area damage in C. uvifera and no damage in T. catappa . In neither species was leaf necrosis observed at T 5 (24 h), the temperature at which F v / F m declined by 5%. In both species, temperatures significantly higher than T 50 (24 h) were required for 50% leaf area necrosis to occur. T 50 (14 days) was a better proxy of visible leaf damage than T 50 (24 h).
The relationship between heat‐induced F v / F m decline and tissue necrosis varies among species. In species surveys of leaf thermal tolerances, calibration of the F v / F m assay against the necrosis test is recommended for each species under investigation. F v / F m measurements soon after heat exposure do not reliably predict irreversible heat damage and may thus not be suitable to model and predict the thermostability of tropical forest trees.
... High temperature thresholds are especially important for leaves given the central role they play in CO 2 assimilation and thus plant growth. Plants have evolved two strategies for maintaining leaf function during extreme high temperature exposure-leaf temperature regulation and leaf thermal tolerance ( 6 ). However, our understanding of how these two strategies function under extreme air temperatures (e.g., >45 °C) remains unclear, due to the difficulty inherent in either replicating such conditions in controlled environments or conducting field-based measurements during naturally occurring extreme heatwaves ( 7 , 8 ). ...
Increasing heatwaves are threatening forest ecosystems globally. Leaf thermal regulation and tolerance are important for plant survival during heatwaves, though the interaction between these processes and water availability is unclear. Genotypes of the widely distributed foundation tree species Populus fremontii were studied in a controlled common garden during a record summer heatwave—where air temperature exceeded 48 °C. When water was not limiting, all genotypes cooled leaves 2 to 5 °C below air temperatures. Homeothermic cooling was disrupted for weeks following a 72-h reduction in soil water, resulting in leaf temperatures rising 3 °C above air temperature and 1.3 °C above leaf thresholds for physiological damage, despite the water stress having little effect on leaf water potentials. Tradeoffs between leaf thermal safety and hydraulic safety emerged but, regardless of water use strategy, all genotypes experienced significant leaf mortality following water stress. Genotypes from warmer climates showed greater leaf cooling and less leaf mortality after water stress in comparison with genotypes from cooler climates. These results illustrate how brief soil water limitation disrupts leaf thermal regulation and potentially compromises plant survival during extreme heatwaves, thus providing insight into future scenarios in which ecosystems will be challenged with extreme heat and unreliable soil water access.
... However, recent studies on T leaf have provided a strong theoretical and empirical basis for challenging this assumption (Leigh et al., 2012(Leigh et al., , 2017Michaletz et al., 2015Michaletz et al., , 2016Dong et al., 2017). Different studies have shown that leaves can be up to 15°C warmer than the surrounding air and that this DT leaf varies greatly across species and environments (Leuzinger & K€ orner, 2007;Fauset et al., 2018;Kitudom et al., 2022;Tarvainen et al., 2022). Accounting for this thermal decoupling is crucial for understanding and predicting the temperature responses of plants as, for example positive DT leaf can allow them to move closer to their thermal optimum in cold environments (Helliker & Richter, 2008) but also may expose them to stronger heat stress if exceedances of the optimum temperature are aggravated in hot environments (V arhammar et al., 2015;Tarvainen et al., 2022). ...
... Different studies have shown that leaves can be up to 15°C warmer than the surrounding air and that this DT leaf varies greatly across species and environments (Leuzinger & K€ orner, 2007;Fauset et al., 2018;Kitudom et al., 2022;Tarvainen et al., 2022). Accounting for this thermal decoupling is crucial for understanding and predicting the temperature responses of plants as, for example positive DT leaf can allow them to move closer to their thermal optimum in cold environments (Helliker & Richter, 2008) but also may expose them to stronger heat stress if exceedances of the optimum temperature are aggravated in hot environments (V arhammar et al., 2015;Tarvainen et al., 2022). ...
... A commonly used method to assess the latter is to measure the temperature response of the maximum quantum yield of photosystem II based on Chla fluorescence, F v /F m where F v is variable fluorescence and F m is maximum fluorescence (e.g. Krause et al., 2010;Slot et al., 2021;Tarvainen et al., 2022). Temperature response curves obtained are then used to determine different photosynthetic heat tolerance thresholds, such as the temperatures at the onset of steep decline in F v /F m (T crit ) or where F v /F m has declined by 50% (T 50 ) or 95% (T 95 ). ...
Current estimates of temperature effects on plants mostly rely on air temperature, although it can significantly deviate from leaf temperature (Tleaf). To address this, some studies have used canopy temperature (Tcan). However, Tcan fails to capture the fine‐scale variation in Tleaf among leaves and species in diverse canopies.
We used infrared radiometers to study Tleaf and Tcan and how they deviate from air temperature (ΔTleaf and ΔTcan) in multispecies tropical tree plantations at three sites along an elevation and temperature gradient in Rwanda.
Our results showed high Tleaf (up to c. 50°C) and ΔTleaf (on average 8–10°C and up to c. 20°C) of sun‐exposed leaves during 10:00 h–15:00 h, being close to or exceeding photosynthetic heat tolerance thresholds. These values greatly exceeded simultaneously measured values of Tcan and ΔTcan, respectively, leading to strongly overestimated leaf thermal safety margins if basing those on Tcan data. Stomatal conductance and leaf size affected Tleaf and Tcan in line with their expected influences on leaf energy balance.
Our findings highlight the importance of leaf traits for leaf thermoregulation and show that monitoring Tcan is not enough to capture the peak temperatures and heat stress experienced by individual leaves of different species in tropical forest canopies.
... They can only make use of their high photosynthetic capacity if they are also hydraulically efficient, that is, if they have high K plant , g s and transpiration. This can give ES species an advantage under high temperatures thanks to higher transpiratory leaf cooling compared to LS species with lower g s (Vårhammar et al., 2015;Tarvainen et al., 2022). However, higher g s depletes soil water faster, and since g min has been shown to correlate with g s (Machado et al., 2021), ES species may also lose more water than LS species under extreme drought conditions. ...
... Traits often differ between successional groups (Mujawamariya et al., 2021;Manishimwe et al., 2022;Tarvainen et al., 2022;Mujawamariya et al., 2023), and sometimes also between species from different origin elevation . Building on this knowledge, we studied five water-use-related traits with a potential impact on heat and drought tolerance -K plant , g s , g min , ψ o and net drought defoliationin 20 Rwandan tropical tree species. ...
... Higher heat sensitivity in species with low gas exchange may partly be linked to high leaf temperatures causing heat stress when grown in warmer conditions. Leaves will heat up more under sunny conditions if transpiratory cooling is low, and the resulting high leaf temperatures will then reduce photosynthesis through increased stomatal limitations at high leaf-to-air VPD, as well as potentially through negative biochemical effects at temperatures approaching heat tolerance thresholds, as has been indicated by other studies (Vårhammar et al., 2015;Fauset et al., 2018;Tarvainen et al., 2022). Both these processes act to decrease tree functioning and increase the risk of carbon starvation under warmer climate. ...
Plants face a trade‐off between hydraulic safety and growth, leading to a range of water‐use strategies in different species. However, little is known about such strategies in tropical trees and whether different water‐use traits can acclimate to warming.
We studied five water‐use traits in 20 tropical tree species grown at three different altitudes in Rwanda (RwandaTREE): stomatal conductance ( g s ), leaf minimum conductance ( g min ), plant hydraulic conductance ( K plant ), leaf osmotic potential ( ψ o ) and net defoliation during drought. We also explored the links between these traits and growth and mortality data.
Late successional (LS) species had low K plant , g s and g min and, thus, low water loss, while low ψ o helped improve leaf water status during drought. Early successional (ES) species, on the contrary, used more water during both moist and dry conditions and exhibited pronounced drought defoliation. The ES strategy was associated with lower mortality and more pronounced growth enhancement at the warmer sites compared to LS species. While K plant and g min showed downward acclimation in warmer climates, ψ o did not acclimate and g s measured at prevailing temperature did not change.
Due to distinctly different water use strategies between successional groups, ES species may be better equipped for a warmer climate as long as defoliation can bridge drought periods.
... Whether European beech, Norway spruce and Douglas fir will be able to persist in Central European forests under a drying and warming climate, both at the juvenile and adult stage, is primarily dependent on their physiological drought resistance, as determined by various hydraulic key traits such as foliar desiccation tolerance (G min ), the stringency of stomatal regulation and hydraulic safety, as well as rooting patterns and the species' drought recovery potential, which underpins the need for a better understanding of the trees' stress physiology. Most likely, the species' heat resistance will also play an increasing role in future (Tarvainen et al. 2022, Münchinger et al. 2022. While mixing Douglas fir or spruce with beech in future production forests can enhance forest stability by promoting ecosystem services and functions related to economics, nutrient-dynamics and biodiversity, we conclude that mixing is not a key factor that can substantially increase the stand resistance against climate change-induced drought and heat. ...
To increase the resilience of forests to drought and other hazards, foresters are increasingly planting mixed stands. This requires knowledge about the drought response of tree species in pure- and mixed-culture neighborhoods. In addition, drought frequently interacts with continued atmospheric nitrogen (N) deposition. To disentangle these factors for European beech, Norway spruce and Douglas fir, we conducted a replicated three-factorial sapling growth experiment with three moisture levels, (high, medium and low), two N levels (high and ambient) and pure and mixed-culture neighborhoods. We measured biomass, stomatal conductance (GS), shoot water potential (at predawn: ΨPD, midday, and turgor loss point: ΨTLP), branch xylem embolism resistance (Ψ50), and minimum epidermal conductance (Gmin).
The three species differed most with respect to Gmin (10-fold higher in beech than in the conifers), hydroscape area (larger in beech), and the time elapsed to reach stomatal closure (TΨGS90) and ΨTLP (TTLP; shorter in beech), while Ψ50 and ΨTLP were remarkably similar. Neighborhood (pure vs. mixed-culture) influenced biomass production, water status and hydraulic traits, notably GS (higher in Douglas fir, but lower in spruce and beech, in mixtures than pure culture), hydraulic safety margin (smaller for beech in mixtures), and TΨGS90 and TTLP (shorter for spruce in mixture). High N generally increased GS, but no consistent N effects on leaf water status and hydraulic traits were detected, suggesting that neighbor identity had a larger effect on plant water relations than N availability.
We conclude that both tree neighborhood and N availability modulate the drought response of beech, spruce and Douglas fir. Species mixing can alleviate the drought stress of some species, but often by disadvantaging other species. Thus, our study suggests stabilizing and building resilience of production forests against a drier and warmer climate may depend primarily on the right species choice; species mixing can support the agenda.
