Augusto C. Franco

Ecological thresholds at the savanna-forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes.

Fire shapes the distribution of savanna and forest through complex interactions involving climate, resources and species traits. Based on data from central Brazil, we propose that these interactions are governed by two critical thresholds. The fire-resistance threshold is reached when individual trees have accumulated sufficient bark to avoid stem death, whereas the fire-suppression threshold is reached when an ecosystem has sufficient canopy cover to suppress fire by excluding grasses. Surpassing either threshold is dependent upon long fire-free intervals, which are rare in mesic savanna. On high-resource sites, the thresholds are reached quickly, increasing the probability that savanna switches to forest, whereas low-resource sites are likely to remain as savanna even if fire is infrequent. Species traits influence both thresholds; saplings of savanna trees accumulate bark thickness more quickly than forest trees, and are more likely to become fire resistant during fire-free intervals. Forest trees accumulate leaf area more rapidly than savanna trees, thereby accelerating the transition to forest. Thus, multiple factors interact with fire to determine the distribution of savanna and forest by influencing the time needed to reach these thresholds. Future work should decipher multiple environmental controls over the rates of tree growth and canopy closure in savanna.

Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees

Seasonal regulation of leaf water potential (ΨL) was studied in eight dominant woody savanna species growing in Brazilian savanna (Cerrado) sites that experience a 5-month dry season. Despite marked seasonal variation in precipitation and air saturation deficit (D), seasonal differences in midday minimum ΨL were small in all of the study species. Water use and water status were regulated by a combination of plant physiological and architectural traits. Despite a nearly 3-fold increase in mean D between the wet and dry season, a sharp decline in stomatal conductance with increasing D constrained seasonal variation in minimum ΨL by limiting transpiration per unit leaf area (E). The leaf surface area per unit of sapwood area (LA/SA), a plant architectural index of potential constraints on water supply in relation to transpirational demand, was about 1.5–8 times greater in the wet season compared to the dry season for most of the species. The changes in LA/SA from the wet to the dry season resulted from a reduction in total leaf surface area per plant, which maintained or increased total leaf-specific hydraulic conductance (Gt) during the dry season. The isohydric behavior of Cerrado tree species with respect to minimum ΨL throughout the year thus was the result of strong stomatal control of evaporative losses, a decrease in total leaf surface area per tree during the dry season, an increase in total leaf-specific hydraulic conductance, and a tight coordination between gas and liquid phase conductance. In contrast with the seasonal isohydric behavior of minimum ΨL, predawn ΨL in all species was substantially lower during the dry season compared to the wet season. During the dry season, predawn ΨL was more negative than bulk soil Ψ estimated by extrapolating plots of E versus ΨL to E=0. Predawn disequilibrium between plant and soil Ψ was attributable largely to nocturnal transpiration, which ranged from 15 to 22% of the daily total. High nocturnal water loss may also have prevented internal water storage compartments from being completely refilled at night before the onset of transpiration early in the day.

Leaf functional traits of Neotropical savanna trees in relation to seasonal water deficit

The seasonal savannas (cerrados) of Central Brazil are characterized by a large diversity of evergreen and deciduous trees, which do not show a clear differentiation in terms of active rooting depth. Irrespective of the depth of the root system, expansion of new foliage in deciduous species occurs at the end of the dry season. In this study, we examined a suite of leaf traits related to C assimilation, water and nutrients (N, P) in five deciduous and six evergreen trees that were among the dominant families of cerrado vegetation. Maximum CO2 assimilation on a mass basis (Amass) was significantly correlated with leaf N and P, and specific leaf area (SLA; leaf area per unit of leaf mass). The highest leaf concentrations of both nutrients were measured in the newly mature leaves of deciduous species at the end of the dry period. The differences in terms of leaf N and P between evergreen and deciduous species decreased during the wet season. Deciduous species also invested less in the production of non-photosynthetic leaf tissues and produced leaves with higher SLA and maintained higher water use efficiency. Thus, deciduous species compensated for their shorter leaf payback period by maintaining higher potential payback capacity (higher values of Amass) and lower leaf construction costs (higher SLA). Their short leafless period and the capacity to flush by the end of the dry season may also contribute to offset the longer payback period of evergreen species, although it may involve the higher cost of maintaining a deep-root system or a tight control of plant water balance in the shallow-rooted ones.

Constraints to seedling success of savanna and forest trees across the savanna-forest boundary

Tropical savannas and closed forests are characterized by distinct tree communities, with most species occurring almost exclusively in only one of the two environments. The ecology of these two groups of species will largely determine the structure and dynamics of the savanna-forest boundary, but little is known about the ecological and physiological differences that might control their distributions. We performed field and nursery experiments to compare seedling establishment success, predawn leaf water potential, biomass allocation, and root carbohydrate concentration of congeneric species, each composed of one savanna species and one forest species. Seedling establishment of savanna and forest species responded differently to vegetation cover, with forest species having lowest establishment success in the open savanna and savanna species having lowest success in forest. Subsequent survival followed similar patterns, resulting in even greater differences in cumulative success. The low survival of forest species in the savanna appears related to drought stress, as seedlings of forest species had lower predawn leaf water potential than savanna species. Seedlings of savanna species had greater root: shoot ratios and root total nonstructural carbohydrate (TNC) concentration, particularly among evergreen genera. Among evergreen genera, root TNC per shoot mass, which may largely determine resprout capacity, was seven times higher in savanna species than forest species. Although water availability and microclimate may reduce the success of forest species, these factors appear unable to completely exclude forest seedling establishment in savanna. Fire, on the other hand, appears to be a much more absolute constraint to success of forest species in savanna.

Interactions between seedlings of Agave deserti and the nurse plant Hilaria rigida

Seedlings of the succulent crassulacean acid metabolism (CAM) plant Agave deserti in the northwestern Sonoran Desert were found only in sheltered microhabitats, nearly all occurring under the canopy of a desert bunchgrass, Hilaria rigida. Apparently because soil surface temperatures can reach 71 0C in exposed areas, seedlings were generally located near the center or on the northern side of this nurse plant. Both species have shallow root systems, about half of the roots of H. rigida and all those for seedlings of A. deserti occurring above soil depths of 0.08 m. To examine competition for water between the nurse plant and an associated seedling, a three-dimensional model for root water uptake was developed. The model divided the soil into 17 concentric sheaths each subdivided radially into eight wedges and vertically into nine layers. Predicted pre-dawn soil water potentials at the mean root depth and total shoot transpiration agreed well with field measurements. Simulated annual water uptake by a seedling of A. deserti was reduced 50% when the seedling was moved from an exposed location to the center of the nurse plant. Shading by the nurse plant reduced total daily photosynthetically active radiation (PAR) by up to 74% compared with an exposed seedling. On the other hand, soil nitrogen under the canopy of H. rigida was 60% higher than in exposed locations. Assuming that the effects of nitrogen, temperature, PAR, and soil water on net CO2 uptake are multiplicative, the predicted net CO2 uptake by a seedling of A. deserti under the nurse plant was only -45% of that for an exposed seedling. Thus, although the nurse plant facilitates seedling establishment by reducing maximum soil surface temperatures and provides a microhabitat with higher soil nitrogen levels, its shading and competition for water reduce seedling growth.

Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems.

Leaf and stem functional traits related to plant water relations were studied for six congeneric species pairs, each composed of one tree species typical of savanna habitats and another typical of adjacent forest habitats, to determine whether there were intrinsic differences in plant hydraulics between these two functional types. Only individuals growing in savanna habitats were studied. Most stem traits, including wood density, the xylem water potential at 50% loss of hydraulic conductivity, sapwood area specific conductivity, and leaf area specific conductivity did not differ significantly between savanna and forest species. However, maximum leaf hydraulic conductance (Kleaf) and leaf capacitance tended to be higher in savanna species. Predawn leaf water potential and leaf mass per area were also higher in savanna species in all congeneric pairs. Hydraulic vulnerability curves of stems and leaves indicated that leaves were more vulnerable to drought-induced cavitation than terminal branches regardless of genus. The midday Kleaf values estimated from leaf vulnerability curves were very low implying that daily embolism repair may occur in leaves. An electric circuit analog model predicted that, compared to forest species, savanna species took longer for their leaf water potentials to drop from predawn values to values corresponding to 50% loss of Kleaf or to the turgor loss points, suggesting that savanna species were more buffered from changes in leaf water potential. The results of this study suggest that the relative success of savanna over forest species in savanna is related in part to their ability to cope with drought, which is determined more by leaf than by stem hydraulic traits. Variation among genera accounted for a large proportion of the total variance in most traits, which indicates that, despite different selective pressures in savanna and forest habitats, phylogeny has a stronger effect than habitat in determining most hydraulic traits.

Midday depression in savanna trees: coordinated adjustments in photochemical efficiency, photorespiration, CO2 assimilation and water use efficiency

High irradiances, high air temperatures and low relative humidities characterize the seasonal savannas of central Brazil, locally known as cerrados. In the present study, we investigated the implications to photoprotection of diurnal adjustments in photochemical and non-photochemical processes in five cerrado woody species that differed in photosynthetic capacity and in the duration and extension of the midday depression of photosynthesis. We also evaluated the contribution of photorespiration to minimize the danger of photoinhibition and the potential carbon costs of the operation of this mechanism in response to changes in irradiance levels. Notwithstanding the large differences in diurnal patterns of photosynthesis and in stomatal conductance, four out of the five species showed a tight common linear relationship between net CO2 assimilation rates and transpiration over the large range of environmental conditions that prevailed during typical sunny days at the end of the rainy season. Large reversible decreases in photochemical efficiency were compensated by proportional increases in non-photochemical processes related to photoprotection, irrespective of the prevailing irradiance levels and degree of stomata closure. Light response curves were used to evaluate the relative contribution of photorespiratory CO2 production to electron flow in response to changes in irradiance levels. A large percentage of the electron flow was used to drive photorespiration in light-saturated leaves. In conclusion, an efficient control of photochemical and non-photochemical quenching and adjustments in the partition of electron flow between assimilative and non-assimilative processes alleviated the danger of photoinhibition. However, the results also suggest that losses in potential carbon gain because of high photorespiratory costs could impose strong limitations on leaf carbon balance of cerrado woody species.

Seasonal patterns of gas exchange, water relations and growth of it Roupala montana, an evergreen savanna species

Roupala montana is an evergreen species widespread in the seasonal savannas of the central plains of Brazil. I examined the degree of coupling of photosynthetic gas-exchange characteristics, water relations and growth responses of R. montana with regard to seasonal changes in soil water availability. Despite a rainless period of over three months soil water potential at 60 cm depth reached values of only about -1.0 MPa, while pre-dawn leaf water potential (Ψl) reached about -0.4 MPa by the end of the three-month drought. Thus, R. montana had access to deep soil water in the dry period, but pre-dawn Ψl did not reach the high wet season values of -0.2 MPa. Most of the shoot growth was concluded in the onset of the rainy season. Although some individual branches might have shown some extension thereafter, most of them remained inactive during the rest of the rainy season and the subsequent dry season. New leaf production was also restricted to the first part of the wet period. R. montana remained evergreen in the dry season, but there was a 27% decrease in the number of leaves and herbivory removed about 16% of the leaf area still present in the plant. CO2-exchange rates of these leaves reached only ca. 55% of the maximum rainy season values of 14 µmol m-2 s-1. Thus, the estimated potential daily carbon gain was about 34% of the maximum by the end of the dry period. These values will be even lower, if we considered the decrease in photosynthetic rates that occurred around midday. These reductions in photosynthetic rates as a result of partial stomatal closure were measured both in the wet and dry season and they were related to increases in the evaporative demand of the atmosphere. In conclusion, the combined effect of herbivory, leaf loss and reductions in photosynthetic rates limited plant productivity in the dry season.

Effects of plant size and water relations on gas exchange and growth of the desert shrub Larrea tridentata

Larrea tridentata is a xerophytic evergreen shrub, dominant in the arid regions of the southwestern United States. We examined relationships between gasexchange characteristics, plant and soil water relations, and growth responses of large versus small shrubs of L. tridentata over the course of a summer growing season in the Chihuahuan Desert of southern New Mexico, USA. The soil wetting front did not reach 0.6 m, and soils at depths of 0.6 and 0.9 m remained dry throughout the summer, suggesting that L. tridentata extracts water largely from soil near the surface. Surface soil layers (<0.3 m) were drier under large plants, but predawn xylem water potentials were similar for both plant sizes suggesting some access to deeper soil moisture reserves by large plants. Stem elongation rates were about 40% less in large, reproductively active shrubs than in small, reproductively inactive shrubs. Maximal net photosynthetic rates (Pmax) occurred in early summer (21.3 μ mol m-2 s-1), when pre-dawn xylem water potential (XWP) reached ca. -1 MPa. Although both shrub sizes exhibited similar responses to environmental factors, small shrubs recovered faster from short-term drought, when pre-dawn XWP reached about -4.5 MPa and Pmax decreased to only ca. 20% of unstressed levels. Gas exchange measurements yielded a strong relationship between stomatal conductance and photosynthesis, and the relationship between leaf-to-air vapor pressure deficit and stomatal conductance was found to be influenced by pre-dawn XWP. Our results indicate that stomatal responses to water stress and vapor pressure deficit are important in determining rates of carbon gain and water loss in L. tridentata.

Photosynthesis of mistletoes in relation to their hosts at various sites in tropical Brazil

Abstract Chlorophyll a fluorescence parameters showing the instantaneous performance and carbon-isotope ratios reflecting long-term behaviour of leaves were determined for a large number of mistletoe/host-pairs in the cerrado belt of Brazil. Study sites were a very exposed rupestrian field, a semi-exposed savanna and a highly shaded gallery forest. The major question asked was if photosynthetic capacity of mistletoe leaves differed from that of the leaves of their respective hosts. It is shown that except for the very exposed rupestrian field site, photosynthetic capacity appeared to be similar in mistletoes and host leaves. The superior behaviour of host leaves in the rupestrian field was due to particularly expressed sun-plant characteristics of the host. However, mistletoes always had higher average stomatal conductances, lower leaf temperatures at similar or even higher irradiance and higher intercellular CO2-partial pressures than hosts. Photosynthetic performance of mistletoe leaves was independent of whether a given mistletoe species parasitized aluminium-accumulating or non-accumulating host species in the cerrados with their aluminium-rich soils.