Effects of leaf silicon on drought performance of tropical tree seedlings.

Elevated leaf silicon (Si) concentrations improve drought resistance in cultivated plants, suggesting Si might also improve drought performance of wild species. Tropical tree species, for instance, take up substantial amounts of Si, and leaf Si varies markedly at local and regional scales, suggesting consequences for seedling drought resistance. Yet, whether elevated leaf Si improves seedling drought performance in tropical forests is unknown. To manipulate leaf Si concentrations, seedlings of seven tropical tree species were grown in Si-rich and -poor soil, before exposing them to drought in the forest understorey. Survival, growth and wilting were monitored. Elevated leaf Si did not improve drought survival and growth in any of the species. In one species, drought survival was reduced in seedlings previously grown in Si-rich soil, contrary to our expectation. Our results suggest that elevated leaf Si does not improve drought resistance of wild tropical tree species. Elevated leaf Si may even reduce drought performance, suggesting differences in soil conditions influencing leaf Si may contribute to soil-related variation of tropical seedling performance. Furthermore, our results are at odds with most studies on cultivated species and show that alleviative effects of Si in crops cannot be generalized to wild plants in natural systems.

Silicon-based anti-herbivore defense in tropical tree seedlings.

Silicon-based defenses deter insect herbivores in many cultivated and wild grass species. Furthermore, in some of these species, silicon (Si) uptake and defense can be induced by herbivory. Tropical trees also take up Si and leaf Si concentrations vary greatly across and within species. As herbivory is a major driver of seedling mortality and niche differentiation of tropical tree species, understanding anti-herbivore defenses is pivotal. Yet, whether silicon is a constitutive and inducible herbivory defense in tropical forest tree species remains unknown. We grew seedlings of eight tropical tree species in a full factorial experiment, including two levels of plant-available soil Si concentrations (-Si/+Si) and a simulated herbivory treatment (-H/+H). The simulated herbivory treatment was a combination of clipping and application of methyl jasmonate. We then carried out multiple-choice feeding trials, separately for each tree species, in which leaves of each treatment combination were offered to a generalist caterpillar (Spodoptera frugiperda). Leaf damage was assessed. Three species showed a significant decrease in leaf damage under high compared to low Si conditions (by up to 72%), consistent with our expectation of Si-based defenses acting in tropical tree species. In one species, leaf damage was increased by increasing soil Si and in four species, no effect of soil Si on leaf damage was observed. Opposite to our expectation of Si uptake and defense being inducible by herbivory damage, simulated herbivory increased leaf damage in two species. Furthermore, simulated herbivory reduced Si concentrations in one species. Our results showed that tropical tree seedlings can be better defended when growing in Si-rich compared to Si-poor soils, and that the effects of Si on plant defense vary strongly across species. Furthermore, Si-based defenses may not be inducible in tropical tree species. Overall, constitutive Si-based defense should be considered part of the vast array of anti-herbivore defenses of tropical tree species. Our finding that Si-based defenses are highly species-specific combined with the fact that herbivory is a major driver of mortality in tropical tree seedling, suggests that variation in soil Si concentrations may have pervasive consequences for regeneration and performance across tropical tree species.

Nutrient effects on drought responses vary across common temperate grassland species.

Drought and nutrient input are two main global change drivers that threaten ecosystem function and services. Resolving the interactive effects of human-induced stressors on individual species is necessary to improve our understanding of community and ecosystem responses. This study comparatively assessed how different nutrient conditions affect whole-plant drought responses across 13 common temperate grassland species. We conducted a fully factorial drought-fertilization experiment to examine the effect of nutrient addition [nitrogen (N), phosphorus (P), and combined NP] on species' drought survival, and on drought resistance of growth as well as drought legacy effects. Drought had an overall negative effect on survival and growth, and the adverse drought effects extended into the next growing season. Neither drought resistance nor legacy effects exhibited an overall effect of nutrients. Instead, both the size and the direction of the effects differed strongly among species and between nutrient conditions. Consistently, species performance ranking under drought changed with nitrogen availability. The idiosyncratic responses of species to drought under different nutrient conditions may underlie the seemingly contradicting effects of drought in studies on grassland composition and productivity along nutrient and land-use gradients-ranging from amplifying to dampening. Differential species' responses to combinations of nutrients and drought, as observed in our study, complicate predictions of community and ecosystem responses to climate and land-use changes. Moreover, they highlight the urgent need for an improved understanding of the mechanisms that render species more or less vulnerable to drought under different nutrients.

Turgor loss point predicts survival responses to experimental and natural drought in tropical tree seedlings.

Identifying key traits that can serve as proxies for species drought resistance is crucial for predicting and mitigating the effects of climate change in diverse plant communities. Turgor loss point (πtlp ) is a recently emerged trait that has been linked to species distributions across gradients of water availability. However, a direct relationship between πtlp and species ability to survive drought has yet to be established for woody species. Using a manipulative field experiment to quantify species drought resistance (i.e., their survival response to drought), combined with measurements of πtlp for 16 tree species, we show a negative relationship between πtlp and seedling drought resistance. Using long-term forest plot data, we also show that πtlp predicts seedling survival responses to a severe El Niño-related drought, although additional factors are clearly also important. Our study demonstrates that species with lower πtlp exhibit higher survival under both experimental and natural drought. These results provide a missing cornerstone in the assessment of the traits underlying drought resistance in woody species and strengthen πtlp as a proxy for evaluating which species will lose or win under projections of exacerbating drought regimes.

Increased mortality of tropical tree seedlings during the extreme 2015-16 El Niño.

As extreme climate events are predicted to become more frequent because of global climate change, understanding their impacts on natural systems is crucial. Tropical forests are vulnerable to droughts associated with extreme El Niño events. However, little is known about how tropical seedling communities respond to El Niño-related droughts, even though patterns of seedling survival shape future forest structure and diversity. Using long-term data from eight tropical moist forests spanning a rainfall gradient in central Panama, we show that community-wide seedling mortality increased by 11% during the extreme 2015-16 El Niño, with mortality increasing most in drought-sensitive species and in wetter forests. These results indicate that severe El Niño-related droughts influence understory dynamics in tropical forests, with effects varying both within and across sites. Our findings suggest that predicted increases in the frequency of extreme El Niño events will alter tropical plant communities through their effects on early life stages.

Variation of foliar silicon concentrations in temperate forbs: effects of soil silicon, phylogeny and habitat.

Silicon (Si) accumulation is known to alleviate various biotic and abiotic stressors in plants with potential ecological consequences. However, for dicotyledonous plants our understanding of Si variation remains limited. We conducted a comparative experimental study to investigate (1) interspecific variation of foliar Si concentrations across 37 dicotyledonous forbs of temperate grasslands, (2) intraspecific variation in foliar Si concentration in response to soil Si availability, the influence of (3) phylogenetic relatedness, and (4) habitat association to moisture. Foliar Si differed markedly (approx. 70-fold) across the investigated forbs, with some species exhibiting Si accumulation similar to grasses. Foliar Si increased with soil Si availability, but the response varied across species: species with higher Si accumulation capacity showed a stronger response, indicating that they did not actively upregulate Si uptake under low soil Si availability. Foliar Si showed a pronounced phylogenetic signal, i.e., closely related species exhibited more similar foliar Si concentrations than distantly related species. Significant differences in foliar Si concentration within closely related species pairs nevertheless support that active Si uptake and associated high Si concentrations has evolved multiple times in forbs. Foliar Si was not higher in species associated with drier habitats, implying that in dicotyledonous forbs of temperate grasslands high foliar Si is not an adaptive trait to withstand drought. Our results demonstrated considerable inter- and intraspecific variation in foliar Si concentration in temperate forbs. This variation should have pervasive, but so far understudied, ecological consequences for community composition and functioning of temperate grasslands under land-use and climate change.

Rethinking the Plant Economics Spectrum for Annuals: A Multi-Species Study.

The plant economics spectrum hypothesizes a correlation among resource-use related traits along one single axis, which determines species' growth rates and their ecological filtering along resource gradients. This concept has been mostly investigated and shown in perennial species, but has rarely been tested in annual species. Annuals evade unfavorable seasons as seeds and thus may underlie different constraints, with consequences for interspecific trait-trait, trait-growth, and trait-environment relations. To test the hypotheses of the plant economics spectrum in annual species, we measured twelve resource-use related leaf and root traits in 30 winter annuals from Israel under controlled conditions. Traits and their coordinations were related to species' growth rates (for 19 species) and their distribution along a steep rainfall gradient. Contrary to the hypotheses of the plant economics spectrum, in the investigated annuals traits were correlated along two independent axes, one of structural traits and one of carbon gain traits. Consequently, species' growth rates were related to carbon gain traits, but independent from structural traits. Species' distribution along the rainfall gradient was unexpectedly neither associated with species' scores along the axes of carbon gain or structural traits nor with growth rate. Nevertheless, root traits were related with species' distribution, indicating that they are relevant for species' filtering along rainfall gradients in winter annuals. Overall, our results showed that the functional constraints hypothesized by the plant economics spectrum do not apply to winter annuals, leading to unexpected trait-growth and trait-rainfall relations. Our study thus cautions to generalize trait-based concepts and findings between life-history strategies. To predict responses to global change, trait-based concepts should be explicitly tested for different species groups.

Local adaptation to herbivory within tropical tree species along a rainfall gradient.

In tropical forests, insect herbivores exert significant pressure on plant populations. Adaptation to such pressure is hypothesized to be a driver of high tropical diversity, but direct evidence for local adaptation to herbivory in tropical forests is sparse. At the same time, herbivore pressure has been hypothesized to increase with rainfall in the tropics, which could lead to differences among sites in the degree of local adaptation. To assess the presence of local adaptation and its interaction with rainfall, we compared herbivore damage on seedlings of local vs. nonlocal populations at sites differing in moisture availability in a reciprocal transplant experiment spanning a rainfall gradient in Panama. For 13 native tree species, seeds collected from multiple populations along the rainfall gradient were germinated in a shadehouse and then transplanted to experimental sites within the species range. We tracked the proportion of seedlings attacked over 1.5 yr and quantified the percentage of leaf area damaged at the end of the study. Seedlings originating from local populations were less likely to be attacked and experienced lower amounts of herbivore damage than those from nonlocal populations, but only on the wetter end of the rainfall gradient. However, overall herbivore damage was higher at the drier site compared to wetter sites, contrary to expectation. Taken together, these findings support the idea that herbivory can result in local adaptation within tropical tree species; however, the likelihood of local adaptation varies among sites because of environmentally driven differences in investment in defense or herbivore specialization or both.

Comparative drought resistance of temperate grassland species: testing performance trade-offs and the relation to distribution.

To improve projections of consequences of increasing intensity and frequency of drought events for grasslands, we need a thorough understanding of species performance responses to drought, of performance trade-offs and how drought resistance is related to species distributions. However, comparative and quantitative assessments of whole-plant drought resistance that allow to rigorously address these aspects are lacking for temperate grassland species. We conducted a common garden experiment with 40 common temperate grassland species to compare species survival and growth under intense drought and well-irrigated conditions. Overall, survival and growth were significantly reduced under drought, with the effect varying across species. Species ranking of drought damage and survival remained consistent with progressing drought. No performance trade-offs emerged between optimal growth and drought resistance of survival ('growth-stress tolerance' trade-off hypothesis), or between growth under well-watered and dry conditions ('growth rates' trade-off hypothesis). Species local- and large-scale association with moisture (Ellenberg F value and rainfall niche) was not related to their drought resistance. Overall, our results imply that trade-offs and differences of species fundamental drought resistance are not the main drivers of hydrological niche differentiation, species coexistence and their distribution across moisture gradients. The comparative experimental assessment of species whole-plant drought responses we present provides a basis to increase our understanding of current grassland responses to variation of moisture regimes and for projecting consequences of future changes.

Performance of tropical forest seedlings under shade and drought: an interspecific trade-off in demographic responses.

Seedlings in moist tropical forests must cope with deep shade and seasonal drought. However, the interspecific relationship between seedling performance in shade and drought remains unsettled. We quantified spatiotemporal variation in shade and drought in the seasonal moist tropical forest on Barro Colorado Island (BCI), Panama, and estimated responses of naturally regenerating seedlings as the slope of the relationship between performance and shade or drought intensity. Our performance metrics were relative height growth and first-year survival. We investigated the relationship between shade and drought responses for up to 63 species. There was an interspecific trade-off in species responses to shade versus species responses to dry season intensity; species that performed worse in the shade did not suffer during severe dry seasons and vice versa. This trade-off emerged in part from the absence of species that performed particularly well or poorly in both drought and shade. If drought stress in tropical forests increases with climate change and as solar radiation is higher during droughts, the trade-off may reinforce a shift towards species that resist drought but perform poorly in the shade by releasing them from deep shade.

Dry season soil water potential maps of a 50 hectare tropical forest plot on Barro Colorado Island, Panama.

Fine scale spatial variation in soil moisture influences plant performance, species distributions and diversity. However, detailed information on local soil moisture variation is scarce, particularly in species-rich tropical forests. We measured soil water potential and soil water content in the 50-ha Forest Dynamics Plot on Barro Colorado Island (BCI), Panama, one of the best-studied tropical forests in the world. We present maps of soil water potential for several dry season stages during a regular year and during an El Niño drought. Additionally, we provide code that allows users to create maps for specific dates. The maps can be combined with other freely available datasets such as long-term vegetation censuses (ranging from seeds to adult trees), data on other resources (e.g. light and nutrients) and remote sensing data (e.g. LiDAR and imaging spectroscopy). Users can study questions in various disciplines such as population and community ecology, plant physiology and hydrology under current and future climate conditions.

The hydraulic efficiency-safety trade-off differs between lianas and trees.

Hydraulic traits are important for woody plant functioning and distribution. Associations among hydraulic traits, other leaf and stem traits, and species' performance are relatively well understood for trees, but remain poorly studied for lianas. We evaluated the coordination among hydraulic efficiency (i.e., maximum hydraulic conductivity), hydraulic safety (i.e., cavitation resistance), a suite of eight morphological and physiological traits, and species' abundances for saplings of 24 liana species and 27 tree species in wet tropical forests in Panama. Trees showed a strong trade-off between hydraulic efficiency and hydraulic safety, whereas efficiency and safety were decoupled in lianas. Hydraulic efficiency was strongly and similarly correlated with acquisitive traits for lianas and trees (e.g., positively with gas exchange rates and negatively with wood density). Hydraulic safety, however, showed no correlations with other traits in lianas, but with several in trees (e.g., positively with leaf dry matter content and wood density and negatively with gas exchange rates), indicating that in lianas hydraulic efficiency is an anchor trait because it is correlated with many other traits, while in trees both efficiency and safety are anchor traits. Traits related to shade tolerance (e.g., low specific leaf area and high wood density) were associated with high local tree sapling abundance, but not with liana abundance. Our results suggest that different, yet unknown mechanisms determine hydraulic safety and local-scale abundance for lianas compared to trees. For trees, the trade-off between efficiency and safety will provide less possibilities for ecological strategies. For lianas, however, the uncoupling of efficiency and safety could allow them to have high hydraulic efficiency, and hence high growth rates, without compromising resistance to cavitation under drought, thus allowing them to thrive and outperform trees under drier conditions.

Effects of Drought, Pest Pressure and Light Availability on Seedling Establishment and Growth: Their Role for Distribution of Tree Species across a Tropical Rainfall Gradient.

Tree species distributions associated with rainfall are among the most prominent patterns in tropical forests. Understanding the mechanisms shaping these patterns is important to project impacts of global climate change on tree distributions and diversity in the tropics. Beside direct effects of water availability, additional factors co-varying with rainfall have been hypothesized to play an important role, including pest pressure and light availability. While low water availability is expected to exclude drought-intolerant wet forest species from drier forests (physiological tolerance hypothesis), high pest pressure or low light availability are hypothesized to exclude dry forest species from wetter forests (pest pressure gradient and light availability hypothesis, respectively). To test these hypotheses at the seed-to-seedling transition, the potentially most critical stage for species discrimination, we conducted a reciprocal transplant experiment combined with a pest exclosure treatment at a wet and a dry forest site in Panama with seeds of 26 species with contrasting origin. Establishment success after one year did not reflect species distribution patterns. However, in the wet forest, wet origin species had a home advantage over dry forest species through higher growth rates. At the same time, drought limited survival of wet origin species in the dry forest, supporting the physiological tolerance hypothesis. Together these processes sort species over longer time frames, and exclude species outside their respective home range. Although we found pronounced effects of pests and some effects of light availability on the seedlings, they did not corroborate the pest pressure nor light availability hypotheses at the seed-to-seedling transition. Our results underline that changes in water availability due to climate change will have direct consequences on tree regeneration and distributions along tropical rainfall gradients, while indirect effects of light and pests are less important.

Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees.

Tropical forest vegetation is shaped by climate and by soil, but understanding how the distributions of individual tree species respond to specific resources has been hindered by high diversity and consequent rarity. To study species over an entire community, we surveyed trees and measured soil chemistry across climatic and geological gradients in central Panama and then used a unique hierarchical model of species occurrence as a function of rainfall and soil chemistry to circumvent analytical difficulties posed by rare species. The results are a quantitative assessment of the responses of 550 tree species to eight environmental factors, providing a measure of the importance of each factor across the entire tree community. Dry-season intensity and soil phosphorus were the strongest predictors, each affecting the distribution of more than half of the species. Although we anticipated clear-cut responses to dry-season intensity, the finding that many species have pronounced associations with either high or low phosphorus reveals a previously unquantified role for this nutrient in limiting tropical tree distributions. The results provide the data necessary for understanding distributional limits of tree species and predicting future changes in forest composition.

Resource limitation, tolerance, and the future of ecological plant classification.

Throughout the evolutionary history of plants, drought, shade, and scarcity of nutrients have structured ecosystems and communities globally. Humans have begun to drastically alter the prevalence of these environmental factors with untold consequences for plant communities and ecosystems worldwide. Given limitations in using organ-level traits to predict ecological performance of species, recent advances using tolerances of low resource availability as plant functional traits are revealing the often hidden roles these factors have in structuring communities and are becoming central to classifying plants ecologically. For example, measuring the physiological drought tolerance of plants has increased the predictability of differences among species in their ability to survive drought as well as the distribution of species within and among ecosystems. Quantifying the shade tolerance of species has improved our understanding of local and regional species diversity and how species have sorted within and among regions. As the stresses on ecosystems continue to shift, coordinated studies of whole-plant growth centered on tolerance of low resource availability will be central in predicting future ecosystem functioning and biodiversity. This will require efforts that quantify tolerances for large numbers of species and develop bioinformatic and other techniques for comparing large number of species.

Functional traits and the growth-mortality trade-off in tropical trees.

A trade-off between growth and mortality rates characterizes tree species in closed canopy forests. This trade-off is maintained by inherent differences among species and spatial variation in light availability caused by canopy-opening disturbances. We evaluated conditions under which the trade-off is expressed and relationships with four key functional traits for 103 tree species from Barro Colorado Island, Panama. The trade-off is strongest for saplings for growth rates of the fastest growing individuals and mortality rates of the slowest growing individuals (r2 = 0.69), intermediate for saplings for average growth rates and overall mortality rates (r2 = 0.46), and much weaker for large trees (r2 < or = 0.10). This parallels likely levels of spatial variation in light availability, which is greatest for fast- vs. slow-growing saplings and least for large trees with foliage in the forest canopy. Inherent attributes of species contributing to the trade-off include abilities to disperse, acquire resources, grow rapidly, and tolerate shade and other stresses. There is growing interest in the possibility that functional traits might provide insight into such ecological differences and a growing consensus that seed mass (SM), leaf mass per area (LMA), wood density (WD), and maximum height (H(max)) are key traits among forest trees. Seed mass, LMA, WD, and H(max) are predicted to be small for light-demanding species with rapid growth and mortality and large for shade-tolerant species with slow growth and mortality. Six of these trait-demographic rate predictions were realized for saplings; however, with the exception of WD, the relationships were weak (r2 < 0.1 for three and r2 < 0.2 for five of the six remaining relationships). The four traits together explained 43-44% of interspecific variation in species positions on the growth-mortality trade-off; however, WD alone accounted for > 80% of the explained variation and, after WD was included, LMA and H(max) made insignificant contributions. Virtually the full range of values of SM, LMA, and H(max) occurred at all positions on the growth-mortality trade-off. Although WD provides a promising start, a successful trait-based ecology of tropical forest trees will require consideration of additional traits.

Seasonal and spatial variation in water availability drive habitat associations in a tropical forest.

Associations with topographic units or soil types that vary in water availability are widespread in plant communities and are one of the main structuring aspects for local species distribution patterns, yet the underlying mechanisms are poorly understood. We hypothesized that differential seedling performance across habitats, particularly during the dry season, leads to habitat associations in seasonal tropical forests. We expected this pattern to be most pronounced in particularly dry years, such as those associated with El Niño Southern Oscillation (ENSO) events. We assessed performance of 36 native tree and shrub species in a moist forest in central Panama across the dry and wet seasons in two topographic habitat types during a year in which dry-season precipitation was reduced due to an ENSO event. At the community level, we found lower growth and higher mortality in the dry season relative to the wet season and higher mortality in the drier plateau habitat relative to the wetter slope habitat. There was large variation in species' responses to season and habitat. Species' mortality and growth rates were significantly correlated with experimentally assessed drought sensitivity, but only during the dry season in the plateau habitat. Slope specialists had significantly higher survival, but not growth, in the slope vs. plateau habitat during the dry season. In contrast, plateau specialists showed no performance differences between habitats. The data suggest that associations with plateau habitats result from a numerical advantage of drought-tolerant species in dry habitats in which seedlings of drought-sensitive species are unable to persist. Overall, our results support the idea that seasonal and spatial variation in water availability, particularly in dry years, drive seedling dynamics, which in turn shape local species distributions. Predicted shifts in rainfall patterns caused by global and regional climate change are therefore expected to alter the dynamics, composition, and diversity of seasonal tropical forests.

When sex is not enough: ecological correlates of resprouting capacity in congeneric tropical forest shrubs.

In moist tropical forests resprouting may be an important component of life history, contributing to asexual reproduction through the clonal spread of individuals derived from shoot fragments. However, in contrast to other ecosystems where resprouting is common, the ecological correlates of resprouting capacity in tropical forests remain largely unexplored. In this study we characterized shade tolerance, resprouting capacity and sexual reproductive success of eight co-occurring Piper species from lowland forests of Panama. In field experiments we found that shade-tolerant Piper species had a higher capacity to regenerate from excised or pinned stem fragments than light-demanding species in both gap and understory light conditions. In contrast, shade-tolerant species had lower recruitment probabilities from seeds, as a consequence of lower initial seed viability, and lower seedling emergence rates. All Piper species needed gap conditions for successful seedling establishment. Of 8,000 seeds sown in the understory only 0.2% emerged. In gaps, seed germination of light-demanding species was between 10 and 50%, whereas for shade-tolerant species it was 0.5-9.8%. We propose that the capacity to reproduce asexually from resprouts could be adaptive for shade-tolerant species that are constantly exposed to damage from falling litter in the understory. Resprouting may allow Piper populations to persist and spread despite the high rate of pre-dispersal seed predation and low seed emergence rates. Across Piper species, we detected a trade-off between resprouting capacity and the annual viable seed production per plant but not with annual seed mass produced per plant. This suggests that species differences in sexual reproductive success may not necessarily result from differential resource allocation. Instead we suggest that low sexual reproductive success in the understory may in part reflect reduced genetic diversity in populations undergoing clonal growth, resulting in self-fertilization and in-breeding depression.

Drought sensitivity shapes species distribution patterns in tropical forests.

Although patterns of tree species distributions along environmental gradients have been amply documented in tropical forests, mechanisms causing these patterns are seldom known. Efforts to evaluate proposed mechanisms have been hampered by a lack of comparative data on species' reactions to relevant axes of environmental variation. Here we show that differential drought sensitivity shapes plant distributions in tropical forests at both regional and local scales. Our analyses are based on experimental field assessments of drought sensitivity of 48 species of trees and shrubs, and on their local and regional distributions within a network of 122 inventory sites spanning a rainfall gradient across the Isthmus of Panama. Our results suggest that niche differentiation with respect to soil water availability is a direct determinant of both local- and regional-scale distributions of tropical trees. Changes in soil moisture availability caused by global climate change and forest fragmentation are therefore likely to alter tropical species distributions, community composition and diversity.