Leaf thermal safety margins decline at hotter temperatures in a natural warming 'experiment' in the Amazon.

The threat of rising global temperatures may be especially pronounced for low-latitude, lowland plant species that have evolved under stable climatic conditions. However, little is known about how these species may acclimate to elevated temperatures. Here, we leveraged a strong, steep thermal gradient along a natural geothermal river to assess the ability of woody plants in the Amazon to acclimate to elevated air temperatures. We measured leaf traits in six common tropical woody species along the thermal gradient to investigate whether individuals of these species: acclimate their thermoregulatory traits to maintain stable leaf temperatures despite higher ambient temperatures; acclimate their photosynthetic thermal tolerances to withstand hotter leaf temperatures; and whether acclimation is sufficient to maintain stable leaf thermal safety margins (TSMs) across different growth temperatures. Individuals of three species acclimated their thermoregulatory traits, and three species increased their thermal tolerances with growth temperature. However, acclimation was generally insufficient to maintain constant TSMs. Notwithstanding, leaf health was generally consistent across growth temperatures. Acclimation in woody Amazonian plants is generally too weak to maintain TSMs at high growth temperatures, supporting previous findings that Amazonian plants will be increasingly vulnerable to thermal stress as temperatures rise.

Tropical Trees Will Need to Acclimate to Rising Temperatures-But Can They?

For tropical forests to survive anthropogenic global warming, trees will need to avoid rising temperatures through range shifts and "species migrations" or tolerate the newly emerging conditions through adaptation and/or acclimation. In this literature review, we synthesize the available knowledge to show that although many tropical tree species are shifting their distributions to higher, cooler elevations, the rates of these migrations are too slow to offset ongoing changes in temperatures, especially in lowland tropical rainforests where thermal gradients are shallow or nonexistent. We also show that the rapidity and severity of global warming make it unlikely that tropical tree species can adapt (with some possible exceptions). We argue that the best hope for tropical tree species to avoid becoming "committed to extinction" is individual-level acclimation. Although several new methods are being used to test for acclimation, we unfortunately still do not know if tropical tree species can acclimate, how acclimation abilities vary between species, or what factors may prevent or facilitate acclimation. Until all of these questions are answered, our ability to predict the fate of tropical species and tropical forests-and the many services that they provide to humanity-remains critically impaired.

Variation in the Drought Tolerance of Tropical Understory Plant Communities across an Extreme Elevation and Precipitation Gradient.

Little is known about how differences in water availability within the "super humid" tropics can influence the physiology of understory plant species and the composition of understory plant communities. We investigated the variation in the physiological drought tolerances of hundreds of understory plants in dozens of plant communities across an extreme elevation and precipitation gradient. Specifically, we established 58 understory plots along a gradient of 400-3600 m asl elevation and 1000-6000 mm yr-1 rainfall in and around Manu National Park in southeastern Peru. Within the plots, we sampled all understory woody plants and measured three metrics of physiological leaf drought tolerance-turgor loss point (TLP), cuticular conductance (Gmin), and solute leakage (SL)-and assessed how the community-level means of these three traits related to the mean annual precipitation (MAP) and elevation (along the study gradient, the temperature decreases linearly, and the vapor pressure deficit increases monotonically with elevation). We did not find any correlations between the three metrics of leaf drought tolerance, suggesting that they represent independent strategies for coping with a low water availability. Despite being widely used metrics of leaf drought tolerance, neither the TLP nor Gmin showed any significant relationships with elevation or the MAP. In contrast, SL, which has only recently been developed for use in ecological field studies, increased significantly at higher precipitations and at lower elevations (i.e., plants in colder and drier habitats have a lower average SL, indicating greater drought tolerances). Our results illustrate that differences in water availability may affect the physiology of tropical montane plants and thus play a strong role in structuring plant communities even in the super humid tropics. Our results also highlight the potential for SL assays to be efficient and effective tools for measuring drought tolerances in the field.

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.

Climate Constrains Photosynthetic Strategies in Darwin's Daisies: A Test of the Climatic Variability and Jack-of-All-Trades Hypotheses.

AbstractEmpirical evidence for the climate variability and performance trade-off hypotheses is limited to animals, and it is unclear whether climate constrains the photosynthetic strategies of plants. The plant genus Scalesia Arn. ex Lindl (family Asteraceae), endemic to the Galápagos archipelago, provides an ideal study system to test these hypotheses because of its species with markedly different leaf morphologies that occupy distinct climatic zones. In this study we tested the classic hypotheses that (1) climate constrains leaf size, (2) high climatic temperature variability selects for thermal generalists (i.e., the climate variability hypothesis), and (3) there is a trade-off between the breadth and rate of photosynthetic performance (i.e., jack-of-all-trades but master of none hypothesis). To do this we measured the leaf morphologies and photosynthetic temperature response curves of 11 Scalesia species. In support of a priori predictions, we found that small-leaved Scalesia species were more likely to occupy hotter and drier climates than large-leaved species, there was a positive relationship between climatic temperature variability and the breadth of photosynthetic performance, and photosynthetic performance was negatively correlated with photosynthetic breadth. Our study is among the first to provide evidence for the performance-breadth trade-off hypothesis in photosynthesis, suggesting that climate change may select for photosynthetic thermal generalists.

Limited acclimation of leaf traits and leaf temperatures in a subtropical urban heat island.

The consequences of rising temperatures for trees will vary between species based on their abilities to acclimate their leaf thermoregulatory traits and photosynthetic thermal tolerances. We tested the hypotheses that adult trees in warmer growing conditions (i) acclimate their thermoregulatory traits to regulate leaf temperatures, (ii) acclimate their thermal tolerances such that tolerances are positively correlated with leaf temperature and (iii) that species with broader thermal niche breadths have greater acclimatory abilities. To test these hypotheses, we measured leaf traits and thermal tolerances of seven focal tree species across steep thermal gradients in Miami's urban heat island. We found that some functional traits varied significantly across air temperatures within species. For example, leaf thickness increased with maximum air temperature in three species, and leaf mass per area and leaf reflectance both increased with air temperature in one species. Only one species was marginally more homeothermic than expected by chance due to acclimation of its thermoregulatory traits, but this acclimation was insufficient to offset elevated air temperatures. Thermal tolerances acclimated to higher maximum air temperatures in two species. As a result of limited acclimation, leaf thermal safety margins (TSMs) were narrower for trees in hotter areas. We found some support for our hypothesis that species with broader thermal niches are better at acclimating to maintain more stable TSMs across the temperature gradients. These findings suggest that trees have limited abilities to acclimate to high temperatures and that thermal niche specialists may be at a heightened risk of thermal stress as global temperatures continue to rise.

Rediscovery of Gasteranthusextinctus L.E.Skog & L.P.Kvist (Gesneriaceae) at multiple sites in western Ecuador.

We report the rediscovery of the Critically Endangered cloud forest herb Gasteranthusextinctus, not seen since 1985. In 2019 and 2021, G.extinctus was recorded at five sites in the western foothills of the Ecuadorian Andes, 4-25 km from the type locality at the celebrated Centinela ridge. We describe the species' distribution, abundance, habitat and conservation status and offer recommendations for further research and conservation efforts focused on G.extinctus and the small, disjunct forest remnants it occupies.

Relationships between species richness and ecosystem services in Amazonian forests strongly influenced by biogeographical strata and forest types.

Despite increasing attention for relationships between species richness and ecosystem services, for tropical forests such relationships are still under discussion. Contradicting relationships have been reported concerning carbon stock, while little is known about relationships concerning timber stock and the abundance of non-timber forest product producing plant species (NTFP abundance). Using 151 1-ha plots, we related tree and arborescent palm species richness to carbon stock, timber stock and NTFP abundance across the Guiana Shield, and using 283 1-ha plots, to carbon stock across all of Amazonia. We analysed how environmental heterogeneity influenced these relationships, assessing differences across and within multiple forest types, biogeographic regions and subregions. Species richness showed significant relationships with all three ecosystem services, but relationships differed between forest types and among biogeographical strata. We found that species richness was positively associated to carbon stock in all biogeographical strata. This association became obscured by variation across biogeographical regions at the scale of Amazonia, resembling a Simpson's paradox. By contrast, species richness was weakly or not significantly related to timber stock and NTFP abundance, suggesting that species richness is not a good predictor for these ecosystem services. Our findings illustrate the importance of environmental stratification in analysing biodiversity-ecosystem services relationships.

Montane species track rising temperatures better in the tropics than in the temperate zone.

Many species are responding to global warming by shifting their distributions upslope to higher elevations, but the observed rates of shifts vary considerably among studies. Here, we test the hypothesis that this variation is in part explained by latitude, with tropical species being particularly responsive to warming temperatures. We analyze two independent empirical datasets-shifts in species' elevational ranges, and changes in composition of forest inventory tree plots. Tropical species are tracking rising temperatures 2.1-2.4 times (range shift dataset) and 10 times (tree plot dataset) better than their temperate counterparts. Models predict that for a 100 m upslope shift in temperature isotherm, species at the equator have shifted their elevational ranges 93-96 m upslope, while species at 45° latitude have shifted only 37-42 m upslope. For tree plots, models predict that a 1°C increase in temperature leads to an increase in community temperature index (CTI), a metric of the average temperature optima of tree species within a plot, of 0.56°C at the equator but no change in CTI at 45° latitude (-0.033°C). This latitudinal gradient in temperature tracking suggests that tropical montane communities may be on an "escalator to extinction" as global temperatures continue to rise.

Mature Andean forests as globally important carbon sinks and future carbon refuges.

It is largely unknown how South America's Andean forests affect the global carbon cycle, and thus regulate climate change. Here, we measure aboveground carbon dynamics over the past two decades in 119 monitoring plots spanning a range of >3000 m elevation across the subtropical and tropical Andes. Our results show that Andean forests act as strong sinks for aboveground carbon (0.67 ± 0.08 Mg C ha-1 y-1) and have a high potential to serve as future carbon refuges. Aboveground carbon dynamics of Andean forests are driven by abiotic and biotic factors, such as climate and size-dependent mortality of trees. The increasing aboveground carbon stocks offset the estimated C emissions due to deforestation between 2003 and 2014, resulting in a net total uptake of 0.027 Pg C y-1. Reducing deforestation will increase Andean aboveground carbon stocks, facilitate upward species migrations, and allow for recovery of biomass losses due to climate change.

Photosystem II heat tolerances characterize thermal generalists and the upper limit of carbon assimilation.

The heat tolerance of photosystem II (PSII) may promote carbon assimilation at higher temperatures and help explain plant responses to climate change. Higher PSII heat tolerance could lead to (a) increases in the high-temperature compensation point (Tmax ); (b) increases in the thermal breadth of photosynthesis (i.e. the photosynthetic parameter Ω) to promote a thermal generalist strategy of carbon assimilation; (c) increases in the optimum rate of carbon assimilation Popt and faster carbon assimilation and/or (d) increases in the optimum temperature for photosynthesis (Topt ). To address these hypotheses, we tested if the Tcrit , T50 and T95 PSII heat tolerances were correlated with carbon assimilation parameters for 21 plant species. Our results did not support Hypothesis 1, but we observed that T50 may be used to estimate the upper thermal limit for Tmax at the species level, and that community mean Tcrit may be useful for approximating Tmax . The T50 and T95 heat tolerance metrics were positively correlated with Ω in support of Hypothesis 2. We found no support for Hypotheses 3 or 4. Our study shows that high PSII heat tolerance is unlikely to improve carbon assimilation at higher temperatures but may characterize thermal generalists with slow resource acquisition strategies.

The legacy of biogeographic history on the composition and structure of Andean forests.

The biogeographic origin of species may help to explain differences in average tree height and aboveground biomass (AGB) of tropical mountain forests. After the Andean uplift, small-statured trees should have been among the initial colonizers of the highlands (new cold environment) from the lowland tropics, since these species are pre-adapted to cold conditions with narrow vessels that are relatively resistant to freezing. If the descendants of these small-statured clades continue to dominate tropical highland forests, there will be a high co-occurrence of close relatives at high elevations. In other words, this scenario predicts a systematic decline in tree size, AGB, and phylogenetic diversity with elevation. In contrast, the colonization of Andean forests by some large-statured clades that originated in temperate regions may modify this expectation and promote a mixing of tropical and temperate clades, thereby increasing the phylogenetic diversity in tropical highland forests. This latter scenario predicts an increase or no change of tree size, AGB, and phylogenetic diversity with elevation. We assessed how the historical immigration of large-statured temperate-affiliated tree lineages adapted to cold conditions may have influenced the composition and structure of Andean forests. Specifically, we used 92 0.25-ha forest inventory plots distributed in the tropical Andes Mountains of Colombia to assess the relationship between the phylogenetic diversity and AGB along elevational gradients. We classified tree species as being either "tropical affiliated" or "temperate affiliated" and estimated their independent contribution to forest AGB. We used structural equation modeling to separate the direct and indirect effect of elevation on AGB. We found a hump-shaped relationship of phylogenetic diversity, AGB, and tree size with elevation. The high phylogenetic diversity found between 1,800-2,200 m above sea level (asl) was due to the mixing of highland floras containing many temperate-affiliated species, and lowland floras containing mostly tropical-affiliated species. The high AGB in highland forests, which contrasted with the expected decline of AGB with elevation, was likely due to the significant contribution of temperate-affiliated species. Our findings highlight the lasting importance of biogeographic history on the composition and structure of Andean mountain forests.

Elevation and latitude drives structure and tree species composition in Andean forests: Results from a large-scale plot network.

Our knowledge about the structure and function of Andean forests at regional scales remains limited. Current initiatives to study forests over continental or global scales still have important geographical gaps, particularly in regions such as the tropical and subtropical Andes. In this study, we assessed patterns of structure and tree species diversity along ~ 4000 km of latitude and ~ 4000 m of elevation range in Andean forests. We used the Andean Forest Network (Red de Bosques Andinos, https://redbosques.condesan.org/) database which, at present, includes 491 forest plots (totaling 156.3 ha, ranging from 0.01 to 6 ha) representing a total of 86,964 identified tree stems ≥ 10 cm diameter at breast height belonging to 2341 identified species, 584 genera and 133 botanical families. Tree stem density and basal area increases with elevation while species richness decreases. Stem density and species richness both decrease with latitude. Subtropical forests have distinct tree species composition compared to those in the tropical region. In addition, floristic similarity of subtropical plots is between 13 to 16% while similarity between tropical forest plots is between 3% to 9%. Overall, plots ~ 0.5-ha or larger may be preferred for describing patterns at regional scales in order to avoid plot size effects. We highlight the need to promote collaboration and capacity building among researchers in the Andean region (i.e., South-South cooperation) in order to generate and synthesize information at regional scale.

Functional composition of epiphyte communities in the Colombian Andes.

We identify changes in the functional composition of vascular epiphytes along a tropical elevational gradient with the aim of quantifying the role of climate in determining the assembly of epiphyte communities. We measured seven leaf functional traits (leaf area, specific leaf area, leaf dry-matter content, leaf thickness, force to punch, stomatal density, and potential conductance index) in the 163 most abundant epiphyte species recorded across 10 sites located along an elevational gradient between 60 and 2,900 m above sea level in the Colombian Andes. We grouped the epiphyte species into seven hierarchical functional groups according to their most characteristic leaf traits. Along the elevational gradient, the two main independent leaf trait dimensions that distinguished community assemblages were defined primarily by leaf area-photosynthetic (LAPS) and mass-carbon (LMCS) gradients. Mean annual temperature was the main determinant of species position along LAPS. In contrast, local changes in specific leaf area due to variation in the epiphytes' relative height of attachment was the main determinant of their position along the LMCS. Our findings indicate that epiphytic plant leaves have evolved to optimize and enhance photosynthesis through a leaf area-based strategy and carbon acquisition through investments in construction costs of leaf area per unit of biomass that aim to regulate light capture and tissue development. Given that most studies of plant functional traits neglect vascular epiphytes, our quantification of the multiple dimensions of epiphyte leaf traits greatly augments our understanding of vascular plant function and adaptation to changing environments.

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.

Author Correction: Widespread but heterogeneous responses of Andean forests to climate change.

In Fig. 2 of this Article, the positive part of the y axis scale should read 0, 0.02, 0.04 instead of 0, 0.04, 0.02. This has been corrected online.

Botanic gardens are an untapped resource for studying the functional ecology of tropical plants.

Functional traits are increasingly used to understand the ecology of plants and to predict their responses to global changes. Unfortunately, trait data are unavailable for the majority of plant species. The lack of trait data is especially prevalent for hard-to-measure traits and for tropical plant species, potentially owing to the many inherent difficulties of working with species in remote, hyperdiverse rainforest systems. The living collections of botanic gardens provide convenient access to large numbers of tropical plant species and can potentially be used to quickly augment trait databases and advance our understanding of species' responses to climate change. In this review, we quantitatively assess the availability of trait data for tropical versus temperate species, the diversity of species available for sampling in several exemplar tropical botanic gardens and the validity of garden-based leaf and root trait measurements. Our analyses support the contention that the living collections of botanic gardens are a valuable scientific resource that can contribute significantly to research on plant functional ecology and conservation.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.