New Proposal of Epiphytic Bromeliaceae Functional Groups to Include Nebulophytes and Shallow Tanks.

The Bromeliaceae family has been used as a model to study adaptive radiation due to its terrestrial, epilithic, and epiphytic habits with wide morpho-physiological variation. Functional groups described by Pittendrigh in 1948 have been an integral part of ecophysiological studies. In the current study, we revisited the functional groups of epiphytic bromeliads using a 204 species trait database sampled throughout the Americas. Our objective was to define epiphytic functional groups within bromeliads based on unsupervised classification, including species from the dry to the wet end of the Neotropics. We performed a hierarchical cluster analysis with 16 functional traits and a discriminant analysis, to test for the separation between these groups. Herbarium records were used to map species distributions and to analyze the climate and ecosystems inhabited. The clustering supported five groups, C3 tank and CAM tank bromeliads with deep tanks, while the atmospheric group (according to Pittendrigh) was divided into nebulophytes, bromeliads with shallow tanks, and bromeliads with pseudobulbs. The two former groups showed distinct traits related to resource (water) acquisition, such as fog (nebulophytes) and dew (shallow tanks). We discuss how the functional traits relate to the ecosystems inhabited and the relevance of acknowledging the new functional groups.

Weak crassulacean acid metabolism and other xerophytic adaptive traits in the genus Beaucarnea Lem. (Asparagaceae).

The genus Beaucarnea (Asparagaceae) has economic value as an ornamental plant but also has ecological importance. Nonetheless, habitat, physiological traits and growth parameters of this genus remain largely unknown. We characterized the environmental ranges of Beaucarnea inermis, B. gracilis and B. pliabilis; and screened for the presence of physiological adaptations to drought (biomass allocation, presence of crassulacean acid metabolism [CAM] and its effect on plant water use). We performed experiments in 3- and 5-year-old nursery-grown plants of the three species, measured dry mass accumulation in leaves/stems/roots and screened for CAM using gas exchange, titratable acidity and δ13 C. We performed a second experiment on the water and light use responses of B. pliabilis under drought treatment. We found that B. gracilis was limited to xerophytic scrubs (precipitation >400 mm yr-1 ), while B. pliabilis and B. inermis (precipitation >500 and 700 mm year-1 , respectively) inhabited dry forests. Beaucarnea gracilis had the lowest dry mass and allocation to leaves, while B. inermis showed the opposite pattern. Only B. pliabilis exhibited small but significant acid fluctuations, characterized as weak CAM, along with high proline content. Acid concentration contributed in 2.7% of the daily carbon during the wet season but represented most of the carbon in the dry season, under closed stomata and had an important contribution to osmolality. Thus, CAM is described for the first time in the genus Beaucarnea, but was only present in one of three species, warranting exploration of this metabolism in the remaining species of this genus.

Leaf water δ18O reflects water vapour exchange and uptake by C3 and CAM epiphytic bromeliads in Panama.

The distributions of CAM and C3 epiphytic bromeliads across an altitudinal gradient in western Panama were identified from carbon isotope (δ13C) signals, and epiphyte water balance was investigated via oxygen isotopes (δ18O) across wet and dry seasons. There were significant seasonal differences in leaf water (δ18Olw), precipitation, stored 'tank' water and water vapour. Values of δ18Olw were evaporatively enriched at low altitude in the dry season for the C3 epiphytes, associated with low relative humidity (RH) during the day. Crassulacean acid metabolism (CAM) δ18Olw values were relatively depleted, consistent with water vapour uptake during gas exchange under high RH at night. At high altitude, cloudforest locations, C3 δ18Olw also reflected water vapour uptake by day. A mesocosm experiment with Tillandsia fasciculata (CAM) and Werauhia sanguinolenta (C3) was combined with simulations using a non-steady-state oxygen isotope leaf water model. For both C3 and CAM bromeliads, δ18Olw became progressively depleted under saturating water vapour by day and night, although evaporative enrichment was restored in the C3 W. sanguinolenta under low humidity by day. Source water in the overlapping leaf base 'tank' was also modified by evaporative δ18O exchanges. The results demonstrate how stable isotopes in leaf water provide insights for atmospheric water vapour exchanges for both C3 and CAM systems.

Seasonal and successional dynamics of size-dependent plant demographic rates in a tropical dry forest.

Tropical forests are globally important for biodiversity conservation and climate change mitigation but are being converted to other land uses. Conversion of seasonally dry tropical forests (SDTF) is particularly high while their protection is low. Secondary succession allows forests to recover their structure, diversity and composition after conversion and subsequent abandonment and is influenced by demographic rates of the constituent species. However, how these rates vary between seasons for different plant sizes at different successional stages in SDTF is not known. The effect of seasonal drought may be more severe early in succession, when temperature and radiation are high, while competition and density-dependent processes may be more important at later stages, when vegetation is tall and dense. Besides, the effects of seasonality and successional stage may vary with plant size. Large plants can better compete with small plants for limiting resources and may also have a greater capacity to withstand stress. We asked how size-dependent density, species density, recruitment and mortality varied between seasons and successional stages in a SDTF. We monitored a chronosequence in Yucatan, Mexico, over six years in three 0.1 ha plots in each of three successional stages: early (3-5 years-old), intermediate (18-20 years-old) and advanced (>50 years-old). Recruitment, mortality and species gain and loss rates were calculated from wet and dry season censuses separately for large (diameter > 5 cm) and small (1-5 cm in diameter) plants. We used linear mixed-effects models to assess the effects of successional stage, seasonality and their changes through time on demographic rates and on plant and species density. Seasonality affected demographic rates and density of large plants, which exhibited high wet-season recruitment and species gain rates at the early stage and high wet-season mortality at the intermediate stage, resulting in an increase in plant and species density early in succession followed by a subsequent stabilization. Small plant density decreased steadily after only 5 years of land abandonment, whereas species density increased with successional stage. A decline in species dominance may be responsible for these contrasting patterns. Seasonality, successional stage and their changes through time had a stronger influence on large plants, likely because of large among-plot variation of small plants. Notwithstanding the short duration of our study, our results suggest that climate-change driven decreases in rainy season precipitation may have an influence on successional dynamics in our study forest as strong as, or even stronger than, prolonged or severe droughts during the dry season.

High resilience to extreme climatic changes in the CAM epiphyte Tillandsia utriculata L. (Bromeliaceae).

Climate change is expected to increase the frequency of extreme climatic events, yet few studies have addressed the capacity of plant species to deal with such events. Species that are widespread are predicted to be highly plastic and able to acclimate to highly changing conditions. To study the plasticity in physiological responses of the widely distributed epiphyte Tillandsia utriculata, we transplanted individuals from a coastal scrub and broadleaf evergreen forest to a similar coastal scrub site and forest. After a 45-day acclimation, the plants were moved to a semi-controlled greenhouse at each site, and then subjected to a 20-day drought. Physiological variables were measured during the acclimation and the drought. The individuals of scrub and forest populations had similar relative water content and carbon assimilation in the contrasting conditions of the two transplantation sites despite the high discrepancy between the environments at their original site. Electron transport rates were higher in individuals from the scrub population. Electron transport rates were also higher than estimated from carbon assimilation, suggesting that photorespiration was present. The individuals of the coastal scrub population had a higher capacity to dissipate excess energy this way. The relative distance index of plasticity was high overall, indicating that some traits are highly plastic (titratable acidity, carbon assimilation) in order to maintain the stability of others (maximum quantum yield Fv /Fm and relative water content). We conclude that T. utriculata is a highly plastic species with a high capacity to tolerate extreme environmental changes over a short time.

Legume abundance along successional and rainfall gradients in Neotropical forests.

The nutrient demands of regrowing tropical forests are partly satisfied by nitrogen-fixing legume trees, but our understanding of the abundance of those species is biased towards wet tropical regions. Here we show how the abundance of Leguminosae is affected by both recovery from disturbance and large-scale rainfall gradients through a synthesis of forest inventory plots from a network of 42 Neotropical forest chronosequences. During the first three decades of natural forest regeneration, legume basal area is twice as high in dry compared with wet secondary forests. The tremendous ecological success of legumes in recently disturbed, water-limited forests is likely to be related to both their reduced leaflet size and ability to fix N2, which together enhance legume drought tolerance and water-use efficiency. Earth system models should incorporate these large-scale successional and climatic patterns of legume dominance to provide more accurate estimates of the maximum potential for natural nitrogen fixation across tropical forests.

A δ(15)N assessment of nitrogen deposition for the endangered epiphytic orchid Laelia speciosa from a city and an oak forest in Mexico.

Atmospheric nitrogen deposition poses a major threat to global biodiversity. Tropical epiphytic plants are especially at risk given their reliance on atmospheric sources of nutrients. The leaf, pseudobulb, and root carbon and nitrogen content, C:N ratio, as well as the nitrogen isotopic composition were studied for individuals of Laelia speciosa from a city and from an oak forest in Mexico. The nitrogen content of leaves was similar between the city and the oak forest, reaching 1.3 ± 0.2 % (dry mass). The δ(15)N of leaves, pseudobulbs, and roots reached 5.6 ± 0.2 ‰ in the city, values found in sites exposed to industrial and vehicular activities. The δ(15)N for plant from the oak forest amounted to -3.1 ± 0.3 ‰, which is similar to values measured from sites with low industrial activities. Some orchids such as Laelia speciosa produce a single pseudobulb per year, i.e., a water and nutrient storage organ, so the interannual nitrogen deposition was studied by considering the ten most recent pseudobulbs for plants from either site formed between 2003 and 2012. The C:N ratio of the ten most recent pseudobulbs from the oak forest, as well as that of the pseudobulbs formed before 2010 for plants in the city were indistinguishable from each other, averaging 132.4 ± 6.5, while it was lower for the two most recent pseudobulbs in the city. The δ(15)N values of pseudobulbs from the oak forest averaged ‒4.4 ± 0.1 ‰ for the entire series. The δ(15)N ranged from 0.1 ± 1.6 ‰ for the oldest pseudobulb to 4.7 ± 0.2 ‰ for the pseudobulb formed in the city from 2008 onwards. Isotopic analysis and the C:N ratio for L. speciosa revealed that rates of nitrogen deposition were higher in the city than in the forest. The δ(15)N values of series of pseudobulbs showed that it is possible to track nitrogen deposition over multiple years.

Photoprotection related to xanthophyll cycle pigments in epiphytic orchids acclimated at different light microenvironments in two tropical dry forests of the Yucatan Peninsula, Mexico.

MAIN CONCLUSION: Epiphytic orchids from dry forests of Yucatán show considerable photoprotective plasticity during the dry season, which depends on leaf morphology and host tree deciduousness. Nocturnal retention of antheraxanthin and zeaxanthin was detected for the first time in epiphytic orchids. In tropical dry forests, epiphytes experience dramatic changes in light intensity: photosynthetic photon flux density may be up to an order of magnitude higher in the dry season compared to the wet season. To address the seasonal changes of xanthophyll cycle (XC) pigments and photosynthesis that occur throughout the year, leaves of five epiphytic orchid species were studied during the early dry, dry and wet seasons in a deciduous and a semi-deciduous tropical forests at two vertical strata on the host trees (3.5 and 1.5 m height). Differences in XC pigment concentrations and photosynthesis (maximum quantum efficiency of photosystem II; F v/F m) were larger among seasons than between vertical strata in both forests. Antheraxanthin and zeaxanthin retention reflected the stressful conditions of the epiphytic microhabitat, and it is described here in epiphytes for the first time. During the dry season, both XC pigment concentrations and photosystem II heat dissipation of absorbed energy increased in orchids in the deciduous forest, while F v/F m and nocturnal acidification (ΔH(+)) decreased, clearly as a response to excessive light and drought. Concentrations of XC pigments were higher than those in orchids with similar leaf shape in semi-deciduous forest. There, only Encyclia nematocaulon and Lophiaris oerstedii showed somewhat reduced F v/F m. No changes in ΔH(+) and F v/F m were detected in Cohniella ascendens throughout the year. This species, which commonly grows in forests with less open canopies, showed leaf tilting that diminished light interception. Light conditions in the uppermost parts of the canopy probably limit the distribution of epiphytic orchids and the retention of zeaxanthin can help to cope with light and drought stress in these forests during the dry season.

A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world.

Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that features nocturnal CO2 uptake, facilitates increased water-use efficiency (WUE), and enables CAM plants to inhabit water-limited environments such as semi-arid deserts or seasonally dry forests. Human population growth and global climate change now present challenges for agricultural production systems to increase food, feed, forage, fiber, and fuel production. One approach to meet these challenges is to increase reliance on CAM crops, such as Agave and Opuntia, for biomass production on semi-arid, abandoned, marginal, or degraded agricultural lands. Major research efforts are now underway to assess the productivity of CAM crop species and to harness the WUE of CAM by engineering this pathway into existing food, feed, and bioenergy crops. An improved understanding of CAM has potential for high returns on research investment. To exploit the potential of CAM crops and CAM bioengineering, it will be necessary to elucidate the evolution, genomic features, and regulatory mechanisms of CAM. Field trials and predictive models will be required to assess the productivity of CAM crops, while new synthetic biology approaches need to be developed for CAM engineering. Infrastructure will be needed for CAM model systems, field trials, mutant collections, and data management.

Water vapour isotopic exchange by epiphytic bromeliads in tropical dry forests reflects niche differentiation and climatic signals.

The 18O signals in leaf water (delta18O(lw)) and organic material were dominated by atmospheric water vapour 18O signals (delta18O(vap)) in tank and atmospheric life forms of epiphytic bromeliads with crassulacean acid metabolism (CAM), from a seasonally dry forest in Mexico. Under field conditions, the mean delta18O(lw) for all species was constant during the course of the day and systematically increased from wet to dry seasons (from 0 to +6 per thousand), when relative water content (RWC) diminished from 70 to 30%. In the greenhouse, progressive enrichment from base to leaf tip was observed at low night-time humidity; under high humidity, the leaf tip equilibrated faster with delta18O(vap) than the other leaf sections. Laboratory manipulations using an isotopically depleted water source showed that delta18O(vap) was more rapidly incorporated than liquid water. Our data were consistent with a Craig-Gordon (C-G) model as modified by Helliker and Griffiths predicting that the influx and exchange of delta18O(vap) control delta18O(lw) in certain epiphytic life forms, despite progressive tissue water loss. We use delta18O(lw) signals to define water-use strategies for the coexisting species which are consistent with habitat preference under natural conditions and life form. Bulk organic matter (delta18O(org)) is used to predict the deltaO18(vap) signal at the time of leaf expansion.