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.

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.

Widespread but heterogeneous responses of Andean forests to climate change.

Global warming is forcing many species to shift their distributions upward, causing consequent changes in the compositions of species that occur at specific locations. This prediction remains largely untested for tropical trees. Here we show, using a database of nearly 200 Andean forest plot inventories spread across more than 33.5° latitude (from 26.8° S to 7.1° N) and 3,000-m elevation (from 360 to 3,360 m above sea level), that tropical and subtropical tree communities are experiencing directional shifts in composition towards having greater relative abundances of species from lower, warmer elevations. Although this phenomenon of 'thermophilization' is widespread throughout the Andes, the rates of compositional change are not uniform across elevations. The observed heterogeneity in thermophilization rates is probably because of different warming rates and/or the presence of specialized tree communities at ecotones (that is, at the transitions between distinct habitats, such as at the timberline or at the base of the cloud forest). Understanding the factors that determine the directions and rates of compositional changes will enable us to better predict, and potentially mitigate, the effects of climate change on tropical forests.

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.

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.

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.

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.

Ancient human disturbances may be skewing our understanding of Amazonian forests.

Although the Amazon rainforest houses much of Earth's biodiversity and plays a major role in the global carbon budget, estimates of tree biodiversity originate from fewer than 1,000 forest inventory plots, and estimates of carbon dynamics are derived from fewer than 200 recensus plots. It is well documented that the pre-European inhabitants of Amazonia actively transformed and modified the forest in many regions before their population collapse around 1491 AD; however, the impacts of these ancient disturbances remain entirely unaccounted for in the many highly influential studies using Amazonian forest plots. Here we examine whether Amazonian forest inventory plot locations are spatially biased toward areas with high probability of ancient human impacts. Our analyses reveal that forest inventory plots, and especially forest recensus plots, in all regions of Amazonia are located disproportionately near archaeological evidence and in areas likely to have ancient human impacts. Furthermore, regions of the Amazon that are relatively oversampled with inventory plots also contain the highest values of predicted ancient human impacts. Given the long lifespan of Amazonian trees, many forest inventory and recensus sites may still be recovering from past disturbances, potentially skewing our interpretations of forest dynamics and our understanding of how these forests are responding to global change. Empirical data on the human history of forest inventory sites are crucial for determining how past disturbances affect modern patterns of forest composition and carbon flux in Amazonian forests.

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.

Global climate change increases risk of crop yield losses and food insecurity in the tropical Andes.

One of the greatest current challenges to human society is ensuring adequate food production and security for a rapidly growing population under changing climatic conditions. Climate change, and specifically rising temperatures, will alter the suitability of areas for specific crops and cultivation systems. In order to maintain yields, farmers may be forced to change cultivation practices, the timing of cultivation, or even the type of crops grown. Alternatively, farmers can change the location where crops are cultivated (e.g., to higher elevations) to track suitable climates (in which case the plants will have to grow in different soils), as cultivated plants will otherwise have to tolerate warmer temperatures and possibly face novel enemies. We simulated these two last possible scenarios (for temperature increases of 1.3°C and 2.6°C) in the Peruvian Andes through a field experiment in which several traditionally grown varieties of potato and maize were planted at different elevations (and thus temperatures) using either the local soil or soil translocated from higher elevations. Maize production declined by 21%-29% in response to new soil conditions. The production of maize and potatoes declined by >87% when plants were grown under warmer temperatures, mainly as a result of the greater incidence of novel pests. Crop quality and value also declined under simulated migration and warming scenarios. We estimated that local farmers may experience severe economic losses of up to 2,300 US$ ha-1  yr-1 . These findings reveal that climate change is a real and imminent threat to agriculture and that there is a pressing need to develop effective management strategies to reduce yield losses and prevent food insecurity. Importantly, such strategies should take into account the influences of non-climatic and/or biotic factors (e.g., novel pests) on plant development.

Thermophilization of adult and juvenile tree communities in the northern tropical Andes.

Climate change is expected to cause shifts in the composition of tropical montane forests towards increased relative abundances of species whose ranges were previously centered at lower, hotter elevations. To investigate this process of "thermophilization," we analyzed patterns of compositional change over the last decade using recensus data from a network of 16 adult and juvenile tree plots in the tropical forests of northern Andes Mountains and adjacent lowlands in northwestern Colombia. Analyses show evidence that tree species composition is strongly linked to temperature and that composition is changing directionally through time, potentially in response to climate change and increasing temperatures. Mean rates of thermophilization [thermal migration rate (TMR), °C ⋅ y(-1)] across all censuses were 0.011 °C ⋅ y(-1) (95% confidence interval = 0.002-0.022 °C ⋅ y(-1)) for adult trees and 0.027 °C ⋅ y(-1) (95% confidence interval = 0.009-0.050 °C ⋅ y(-1)) for juvenile trees. The fact that thermophilization is occurring in both the adult and juvenile trees and at rates consistent with concurrent warming supports the hypothesis that the observed compositional changes are part of a long-term process, such as global warming, and are not a response to any single episodic event. The observed changes in composition were driven primarily by patterns of tree mortality, indicating that the changes in composition are mostly via range retractions, rather than range shifts or expansions. These results all indicate that tropical forests are being strongly affected by climate change and suggest that many species will be at elevated risk for extinction as warming continues.

An estimate of the number of tropical tree species.

The high species richness of tropical forests has long been recognized, yet there remains substantial uncertainty regarding the actual number of tropical tree species. Using a pantropical tree inventory database from closed canopy forests, consisting of 657,630 trees belonging to 11,371 species, we use a fitted value of Fisher's alpha and an approximate pantropical stem total to estimate the minimum number of tropical forest tree species to fall between ∼ 40,000 and ∼ 53,000, i.e., at the high end of previous estimates. Contrary to common assumption, the Indo-Pacific region was found to be as species-rich as the Neotropics, with both regions having a minimum of ∼ 19,000-25,000 tree species. Continental Africa is relatively depauperate with a minimum of ∼ 4,500-6,000 tree species. Very few species are shared among the African, American, and the Indo-Pacific regions. We provide a methodological framework for estimating species richness in trees that may help refine species richness estimates of tree-dependent taxa.

Contrasting outcomes of species- and community-level analyses of the temporal consistency of functional composition.

Multiple anthropogenic drivers affect every natural community, and there is broad interest in using functional traits to understand and predict the consequences for future biodiversity. There is, however, no consensus regarding the choice of analytical methods. We contrast species- and community-level analyses of change in the functional composition for four traits related to drought tolerance using three decades of repeat censuses of trees in the 50-ha Forest Dynamics Plot on Barro Colorado Island, Panama. Community trait distributions shifted significantly through time, which may indicate a shift toward more drought tolerant species. However, at the species level, changes in abundance were unrelated to trait values. To reconcile these seemingly contrasting results, we evaluated species-specific contributions to the directional shifts observed at the community level. Abundance changes of just one to six of 312 species were responsible for the community-level shifts observed for each trait. Our results demonstrate that directional changes in community-level functional composition can result from idiosyncratic change in a few species rather than widespread community-wide changes associated with functional traits. Future analyses of directional change in natural communities should combine community-, species-, and possibly individual-level analyses to uncover relationships with function that can improve understanding and enable prediction.

Seedling transplants reveal species-specific responses of high-elevation tropical treeline trees to climate change.

The elevations at which tropical treelines occur are believed to represent the point where low mean temperatures limit the growth of upright woody trees. Consequently, tropical treelines are predicted to shift to higher elevations with global warming. However, treelines throughout the tropics have remained stationary despite increasing global mean temperatures. The goal of the study reported here was to build a more comprehensive understanding of the effects of mean temperature, low-temperature extremes, shading, and their interactions on seedling survival at tropical treelines. We conducted a seedling transplant study using three dominant canopy-forming treeline species in the southern tropical Andes. We found species-specific differences and contrasting responses in seedling survival to changes in mean temperature. The most abundant naturally occurring species at the seedling stage outside the treeline, Weinmannia fagaroides, showed a negative relationship between the survival of transplanted seedlings and mean temperature, the opposite of a priori expectations. Conversely, Clethra cuneata showed increased survival at higher mean temperatures, but survival also increased with higher absolute low temperatures and the presence of shade. Finally, the survival of Gynoxys nitida seedlings was insensitive to temperature but increased under shade. These findings show that multiple factors can determine the upper distributional limit of species forming the current tropical treeline. As such, predictions of future local and regional tropical treeline shifts may need to consider several factors beyond changes in mean temperature. If the treeline remains stationary and cloud forests are unable to expand into higher elevations, there may be severe species loss in this biodiversity hotspot.

Freezing temperatures as a limit to forest recruitment above tropical Andean treelines.

The elevation of altitudinal treelines is generally believed to occur where low mean temperatures during the growing season limit growth and prevent trees from establishing at higher elevations. Accordingly, treelines should move upslope with increasing global temperatures. Contrary to this prediction, tropical treelines have remained stable over the past several decades despite increasing mean temperatures. The observed stability of tropical treelines, coupled with the drastically different temperature profiles between temperate and tropical treelines, suggests that using mean measures of temperature to predict tropical treeline movements during climate change may be overly simplistic. We hypothesize that frost events at tropical treelines may slow climate driven treeline movement by preventing tree recruitment beyond the established forest canopy. To assess this hypothesis, we measured freezing resistance of four canopy-forming treeline species (Weinmannia fagaroides, Polylepis pauta, Clethra cuneata, and Gynoxys nitida) at two life stages (juvenile and adult) and during two seasons (warm-wet and cold-dry). Freezing resistances were then compared to microclimatic data to determine if freezing events in the grassland matrix above treeline are too harsh for these forest species. Freezing resistance varied among species and life stages from -5.7 degrees C for juveniles of P. pauta to -11.1 degrees C for juveniles of W. fagaroides. Over a four-year period, the lowest temperatures recorded at 10 cm above ground level in the grasslands above treeline and at treeline itself were -8.9 degrees C and -6.8 degrees C, respectively. Juveniles maintained freezing resistances similar to adults during the coldest parts of the year and ontogenetic differences in freezing resistance were only present during the warm season when temperatures did not represent a significant threat to active plant tissue. These findings support the hypothesis that rare extreme freezing events at and above tropical treelines can prevent recruitment outside of closed canopy forest for some tree species and may significantly slow treeline advancement despite warming mean temperatures. Predictions of treeline shifts under climate change should be reevaluated to include species-specific' climatic tolerances and measures of climatic variability.

Compositional shifts in Costa Rican forests due to climate-driven species migrations.

Species are predicted to shift their distributions upslope or poleward in response to global warming. This prediction is supported by a growing number of studies documenting species migrations in temperate systems but remains poorly tested for tropical species, and especially for tropical plant species. We analyzed changes in tree species composition in a network of 10 annually censused 1-ha plots spanning an altitudinal gradient of 70-2800 m elevation in Costa Rica. Specifically, we combined plot data with herbarium records (accessed through GBIF) to test if the plots' community temperature scores (CTS, average thermal mean of constituent species weighted by basal area) have increased over the past decade as is predicted by climate-driven species migrations. In addition, we quantified the contributions of stem growth, recruitment, and mortality to the observed patterns. Supporting our a priori hypothesis of upward species migrations, we found that there have been consistent directional shifts in the composition of the plots, such that the relative abundance of lowland species, and hence CTS, increased in 90% of plots. The rate of the observed compositional shifts corresponds to a mean thermal migration rate (TMR) of 0.0065 °C yr(-1) (95% CI = 0.0005-0.0132 °C yr(-1) ). While the overall TMR is slower than predicted based on concurrent regional warming of 0.0167 °C yr(-1) , migrations were on pace with warming in 4 of the 10 plots. The observed shifts in composition were driven primarily by mortality events (i.e., the disproportionate death of highland vs. lowland species), suggesting that individuals of many tropical tree species will not be able to tolerate future warming and thus their persistence in the face of climate change will depend on successful migrations. Unfortunately, in Costa Rica and elsewhere, land area inevitably decreases at higher elevations; hence, even species that are able to migrate successfully will face heightened risks of extinction.

Patterns of bird functional diversity on land-bridge island fragments.

The loss of species diversity due to habitat fragmentation has been extensively studied. In contrast, the impacts of habitat fragmentation on functional diversity remains relatively poorly understood. We conducted bird functional diversity studies on a set of 41 recently isolated land-bridge islands in the Thousand Island Lake, China. We analysed differences in bird species richness and a recently developed suite of complementary functional diversity indices (FRic, volume of functional space occupied; FEve, evenness of abundance distribution in the functional trait space; FDiv, divergence in the distribution of abundance in the trait volume) across different gradients (island area and isolation). We found no correlations between FRic and FEve or FEve and FDiv, but negative correlations between FRic and FDiv. As predicted, island area accounted for most of the variation in bird species richness, whereas isolation explained most of the variation in species evenness (decreasing species evenness with increasing isolation). Functional diversity appears to be more strongly influenced by habitat filtering as opposed to limiting similarity. More specifically, across all islands, both FRic and FEve were significantly lower than expected for randomly assembled communities, but FDiv showed no clear patterns. FRic increased with island area, FEve decreased with island area and FDiv showed no clear patterns. Our finding that FEve decreases with island area at TIL may indicate low functional stability on such islands, and as such large islands and habitat patches may deserve extra attention and/or protection. These results help to demonstrate the importance of considering the effects of fragmentation on functional diversity in habitat management and reserve design plans.