Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms.

Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi-epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi-epiphytic and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (-63%), shorter stipe lengths (-56%), thicker laminae (+41%) and reduced stomatal density (-46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi-epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi-epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely evolutionarily constrained physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat.

Whole-tree mesophyll conductance reconciles isotopic and gas-exchange estimates of water-use efficiency.

Photosynthetic water-use efficiency (WUE) describes the link between terrestrial carbon (C) and water cycles. Estimates of intrinsic WUE (iWUE) from gas exchange and C isotopic composition (δ13 C) differ due to an internal conductance in the leaf mesophyll (gm ) that is variable and seldom computed. We present the first direct estimates of whole-tree gm , together with iWUE from whole-tree gas exchange and δ13 C of the phloem (δ13 Cph ). We measured gas exchange, online 13 C-discrimination, and δ13 Cph monthly throughout spring, summer, and autumn in Eucalyptus tereticornis grown in large whole-tree chambers. Six trees were grown at ambient temperatures and six at a 3°C warmer air temperature; a late-summer drought was also imposed. Drought reduced whole-tree gm . Warming had few direct effects, but amplified drought-induced reductions in whole-tree gm . Whole-tree gm was similar to leaf gm for these same trees. iWUE estimates from δ13 Cph agreed with iWUE from gas exchange, but only after incorporating gm . δ13 Cph was also correlated with whole-tree 13 C-discrimination, but offset by -2.5 ± 0.7‰, presumably due to post-photosynthetic fractionations. We conclude that δ13 Cph is a good proxy for whole-tree iWUE, with the caveats that post-photosynthetic fractionations and intrinsic variability of gm should be incorporated to provide reliable estimates of this trait in response to abiotic stress.

Insights into the evolutionary history and widespread occurrence of antheridiogen systems in ferns.

Sex expression of homosporous ferns is controlled by multiple factors, one being the antheridiogen system. Antheridiogens are pheromones released by sexually mature female fern gametophytes, turning nearby asexual gametophytes precociously male. Nevertheless, not all species respond. It is still unknown how many fern species use antheridiogens, how the antheridiogen system evolved, and whether it is affected by polyploidy and/or apomixis. We tested the response of 68 fern species to antheridiogens in cultivation. These results were combined with a comprehensive review of literature to form the largest dataset of antheridiogen interactions to date. Analyzed species also were coded as apomictic or sexual and diploid or polyploid. Our final dataset contains a total of 498 interactions involving 208 species (c. 2% of all ferns). About 65% of studied species respond to antheridiogen. Multiple antheridiogen types were delimited and their evolution is discussed. Antheridiogen responsiveness was not significantly affected by apomixis or polyploidy. Antheridiogens are widely used by ferns to direct sex expression. The antheridiogen system likely evolved multiple times and provides homosporous ferns with the benefits often associated with heterospory, such as increased rates of outcrossing. Despite expectations, antheridiogens may be beneficial to polyploids and apomicts.

Responses of respiration in the light to warming in field-grown trees: a comparison of the thermal sensitivity of the Kok and Laisk methods.

The Kok and Laisk techniques can both be used to estimate light respiration Rlight . We investigated whether responses of Rlight to short- and long-term changes in leaf temperature depend on the technique used to estimate Rlight . We grew Eucalyptus tereticornis in whole-tree chambers under ambient temperature (AT) or AT + 3°C (elevated temperature, ET). We assessed dark respiration Rdark and light respiration with the Kok (RKok ) and Laisk (RLaisk ) methods at four temperatures to determine the degree of light suppression of respiration using both methods in AT and ET trees. The ET treatment had little impact on Rdark , RKok or RLaisk . Although the thermal sensitivities of RKok or RLaisk were similar, RKok was higher than RLaisk . We found negative values of RLaisk at the lowest measurement temperatures, indicating positive net CO2 uptake, which we propose may be related to phosphoenolpyruvate carboxylase activity. Light suppression of Rdark decreased with increasing leaf temperature, but the degree of suppression depended on the method used. The Kok and Laisk methods do not generate the same estimates of Rlight or light suppression of Rdark between 20 and 35°C. Negative rates of RLaisk imply that this method may become less reliable at low temperatures.

Convergence of ecophysiological traits drives floristic composition of early lineage vascular plants in a tropical forest floor.

BACKGROUND AND AIMS: Tropical understorey plant communities are highly diverse and characterized by variable resource availability, especially light. Plants in these competitive environments must carefully partition resources to ensure ecological and evolutionary success. One mechanism of effective resource partitioning is the optimization of functional traits to enhance competition in highly heterogeneous habitats. Here, we surveyed the ecophysiology of two early lineage vascular plant groups from a tropical forest understorey: Selaginella (a diverse lineage of lycophytes) and ferns. METHODS: In a lowland rain forest in Costa Rica, we measured a suite of functional traits from seven species of Selaginella and six fern species. We evaluated species microclimate and habitat; several photosynthetic parameters; carbon, nitrogen and phosphorus content; chlorophyll concentration; leaf mass per area (LMA); and stomatal size and density. We then compare these two plant lineages and search for relationships between key functional parameters that already exist on a global scale for angiosperms. KEY RESULTS: Convergence of trait function filtered Selaginella species into different habitats, with species in heavily shaded environments having higher chlorophyll concentrations and lower light compensation points compared with open habitats. Alternatively, lower foliar nitrogen and higher stomatal densities were detected in species occupying these open habitats. Selaginella species had denser and smaller stomata, lower LMA and lower foliar nutrient content than ferns, revealing how these plant groups optimize ecophysiological function differently in tropical forest floors. CONCLUSIONS: Our findings add key pieces of missing evidence to global explorations of trait patterns that define vascular plant form and function, which largely focus on seed plants. Broadly predictable functional trait relationships were detected across both Selaginella and ferns, similar to those of seed plants. However, evolutionary canalization of microphyll leaf development appears to have driven contrasting, yet successful, ecophysiological strategies for two coexisting lineages of extant homosporous vascular plants.

Reduced growth due to belowground sink limitation is not fully explained by reduced photosynthesis.

Sink limitation is known to reduce plant growth, but it is not known how plant carbon (C) balance is affected, limiting our ability to predict growth under sink-limited conditions. We manipulated soil volume to impose sink limitation of growth in Eucalyptus tereticornis Sm. seedlings. Seedlings were grown in the field in containers of different sizes and planted flush to the soil alongside freely rooted (Free) seedlings. Container volume negatively affected aboveground growth throughout the experiment, and light saturated rates of leaf photosynthesis were consistently lower in seedlings in containers (-26%) compared with Free seedlings. Significant reductions in photosynthetic capacity in containerized seedlings were related to both reduced leaf nitrogen content and starch accumulation, indicating direct effects of sink limitation on photosynthetic downregulation. After 120 days, harvested biomass of Free seedlings was on average 84% higher than seedlings in containers, but biomass distribution in leaves, stems and roots was not different. However, the reduction in net leaf photosynthesis over the growth period was insufficient to explain the reduction in growth, so that we also observed an apparent reduction in whole-plant C-use efficiency (CUE) between Free seedlings and seedlings in containers. Our results show that sink limitation affects plant growth through feedbacks to both photosynthesis and CUE. Mass balance approaches to predicting plant growth under sink-limited conditions need to incorporate both of these feedbacks.

Coupled response of stomatal and mesophyll conductance to light enhances photosynthesis of shade leaves under sunflecks.

Light gradients within tree canopies play a major role in the distribution of plant resources that define the photosynthetic capacity of sun and shade leaves. However, the biochemical and diffusional constraints on gas exchange in sun and shade leaves in response to light remain poorly quantified, but critical for predicting canopy carbon and water exchange. To investigate the CO2 diffusion pathway of sun and shade leaves, leaf gas exchange was coupled with concurrent measurements of carbon isotope discrimination to measure net leaf photosynthesis (An ), stomatal conductance (gs ) and mesophyll conductance (gm ) in Eucalyptus tereticornis trees grown in climate controlled whole-tree chambers. Compared to sun leaves, shade leaves had lower An , gm , leaf nitrogen and photosynthetic capacity (Amax ) but gs was similar. When light intensity was temporarily increased for shade leaves to match that of sun leaves, both gs and gm increased, and An increased to values greater than sun leaves. We show that dynamic physiological responses of shade leaves to altered light environments have implications for up-scaling leaf level measurements and predicting whole canopy carbon gain. Despite exhibiting reduced photosynthetic capacity, the rapid up-regulation of gm with increased light enables shade leaves to respond quickly to sunflecks.

Elevated carbon dioxide and ozone alter productivity and ecosystem carbon content in northern temperate forests.

Three young northern temperate forest communities in the north-central United States were exposed to factorial combinations of elevated carbon dioxide (CO2 ) and tropospheric ozone (O3 ) for 11 years. Here, we report results from an extensive sampling of plant biomass and soil conducted at the conclusion of the experiment that enabled us to estimate ecosystem carbon (C) content and cumulative net primary productivity (NPP). Elevated CO2 enhanced ecosystem C content by 11%, whereas elevated O3 decreased ecosystem C content by 9%. There was little variation in treatment effects on C content across communities and no meaningful interactions between CO2 and O3 . Treatment effects on ecosystem C content resulted primarily from changes in the near-surface mineral soil and tree C, particularly differences in woody tissues. Excluding the mineral soil, cumulative NPP was a strong predictor of ecosystem C content (r(2) = 0.96). Elevated CO2 enhanced cumulative NPP by 39%, a consequence of a 28% increase in canopy nitrogen (N) content (g N m(-2) ) and a 28% increase in N productivity (NPP/canopy N). In contrast, elevated O3 lowered NPP by 10% because of a 21% decrease in canopy N, but did not impact N productivity. Consequently, as the marginal impact of canopy N on NPP (∆NPP/∆N) decreased through time with further canopy development, the O3 effect on NPP dissipated. Within the mineral soil, there was less C in the top 0.1 m of soil under elevated O3 and less soil C from 0.1 to 0.2 m in depth under elevated CO2 . Overall, these results suggest that elevated CO2 may create a sustained increase in NPP, whereas the long-term effect of elevated O3 on NPP will be smaller than expected. However, changes in soil C are not well-understood and limit our ability to predict changes in ecosystem C content.

Climate change alters seedling emergence and establishment in an old-field ecosystem.

BACKGROUND: Ecological succession drives large-scale changes in ecosystem composition over time, but the mechanisms whereby climatic change might alter succession remain unresolved. Here, we asked if the effects of atmospheric and climatic change would alter tree seedling emergence and establishment in an old-field ecosystem, recognizing that small shifts in rates of seedling emergence and establishment of different species may have long-term repercussions on the transition of fields to forests in the future. METHODOLOGY/PRINCIPAL FINDINGS: We introduced seeds from three early successional tree species into constructed old-field plant communities that had been subjected for 4 years to altered temperature, precipitation, and atmospheric CO(2) regimes in an experimental facility. Our experiment revealed that different combinations of atmospheric CO(2) concentration, air temperature, and soil moisture altered seedling emergence and establishment. Treatments directly and indirectly affected soil moisture, which was the best predictor of seedling establishment, though treatment effects differed among species. CONCLUSIONS: The observed impacts, coupled with variations in the timing of seed arrival, are demonstrated as predictors of seedling emergence and establishment in ecosystems under global change.

Soil ecosystem functioning under climate change: plant species and community effects.

Feedbacks of terrestrial ecosystems to atmospheric and climate change depend on soil ecosystem dynamics. Soil ecosystems can directly and indirectly respond to climate change. For example, warming directly alters microbial communities by increasing their activity. Climate change may also alter plant community composition, thus indirectly altering the soil communities that depend on their inputs. To better understand how climate change may directly and indirectly alter soil ecosystem functioning, we investigated old-field plant community and soil ecosystem responses to single and combined effects of elevated [CO2], warming, and precipitation in Tennessee (USA). Specifically, we collected soils at the plot level (plant community soils) and beneath dominant plant species (plant-specific soils). We used microbial enzyme activities and soil nematodes as indicators for soil ecosystem functioning. Our study resulted in two main findings: (1) Overall, while there were some interactions, water, relative to increases in [CO2] and warming, had the largest impact on plant community composition, soil enzyme activity, and soil nematodes. Multiple climate-change factors can interact to shape ecosystems, but in our study, those interactions were largely driven by changes in water. (2) Indirect effects of climate change, via changes in plant communities, had a significant impact on soil ecosystem functioning, and this impact was not obvious when looking at plant community soils. Climate-change effects on enzyme activities and soil nematode abundance and community structure strongly differed between plant community soils and plant-specific soils, but also within plant-specific soils. These results indicate that accurate assessments of climate-change impacts on soil ecosystem functioning require incorporating the concurrent changes in plant function and plant community composition. Climate-change-induced shifts in plant community composition will likely modify or counteract the direct impact of atmospheric and climate change on soil ecosystem functioning, and hence, these indirect effects should be taken into account when predicting the manner in which global change will alter ecosystem functioning.