Aurelio Virgo

High susceptibility to photoinhibition of young leaves of tropical forest trees

Photoinhibition of photosynthesis was studied in young (but almost fully expanded) and mature canopy sun leaves of several tropical forest tree species, both under controlled conditions (exposure of detached leaves to about 1.8 mmol photons·m-2·s-1) and in the field. The degree of photoinhibition was determined by means of the ratio of variable to maximum chlorophyll (Chl) fluorescence emission (FV/FM) and also by gas-exchange measurements. For investigations in situ, young and mature leaves with similar exposure to sunlight were compared. The results show a consistently higher degree of photoinhibition in the young leaves. In low light, fast recovery was observed in both types of leaves in situ, as well as in the laboratory. The fluorescence parameter 1 — FS/F′M (where FS = stationary fluorescence and f′M = maximum fluorescence during illumination) was followed in situ during the course of the day in order to test its suitability as a measure of the photosynthetic yield of photosystem II (PSII). Electron-transport rates were calculated from these fluorescence signals and compared with rates of net CO2 assimilation. Measurements of diurnal changes in PSII ‘yield’ confirmed the increased susceptibility of young leaves to photoinhibition. Calculated electron transport qualitatively reflected net CO2 uptake in situ during the course of the day. Photosynthetic pigments were analyzed in darkened and illuminated leaves. Young and mature leaves showed the same Chl a/b ratio, but young leaves contained about 50% less Chl a + b per unit leaf area. The capacity of photosynthetic O2 evolution per unit leaf area was decreased to a similar extent in young leaves. On a Chl basis, young leaves contained more α-carotene, more xanthophyll cycle pigments and, under strong illumination, more zeaxanthin than mature leaves. The high degree of reversible photoinhibition observed in these young sun leaves probably represents a dynamic regulatory process protecting the photosynthetic apparatus from severe damage by excess light.

Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest species: a comparative field study on canopy, gap and understory plants

Xanthophyll-cycle pigments and photosynthetic capacity (PSmax) were analyzed in 25 species from different light environments (canopy, gap, understory) within a Panamanian tropical forest. (1) Sun-exposed leaves of canopy tree species showed the highest photosynthetic capacities and largest xanthophyll-cycle pools (violaxanthin, antheraxanthin, zeaxanthin) of about 87 mmol mol-1 chlorophyll with only small amounts of α-carotene [about 7 mmol mol-1 chlorophyll = 8% of total (α+β) carotene pool]. Under high natural photon flux densities (PFDs) canopy leaves rapidly converted up to 96% of the xanthophyll-cycle pool into zeaxanthin. The back reaction to violaxanthin occurred much faster in low light than in complete darkness. At the end of the night, zeaxanthin still accounted for, on average, 14% of the total xanthophyll-cycle pigments. (2) Leaves of gap plants had intermediate values of PSmax and a 43% lower total carotenoid content than canopy leaves. The average size of the xanthophyll-cycle pool was 35 mmol mol-1 chlorophyll, and α-carotene accounted for up to 66% of the total (α+β) carotene pool. Under high light conditions gap plants converted, on average, 86% of the xanthophyll-cycle pigments into zeaxanthin. The back reaction, following a decrease in ambient PFD, was slower than the forward reaction. At the end of the night, zeaxanthin accounted for, on average, 7% of the xanthophyll-cycle pigments in gap plants. (3) Understory plants showed the lowest values of PSmax and the smallest xanthophyll-cycle pool of about 22 mmol mol-1 chlorophyll. α-Carotene accounted for up to 70% of total carotene. The conversion of xanthophyll-cycle pigments into zeaxanthin was negligible during short sunflecks of 1–2 min duration and PFDs up to about 400 μmol m-2 s-1. At predawn, leaves of understory plants rarely contained any detectable zeaxanthin. Aechmea magdalenae, an understory CAM plant, showed exceptionally high rates of PSmax per unit leaf area compared to sympatric C3 understory species.

Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants

A survey of photosynthetic pigments, including 86 species from 64 families, was conducted for leaves of neotropical vascular plants to study sun-shade patterns in carotenoid biosynthesis and occurrence of α-carotene (α-Car) and lutein epoxide (Lx). Under low light, leaves invested less in structural components and more in light harvesting, as manifested by low leaf dry mass per area (LMA) and enhanced mass-based accumulation of chlorophyll (Chl) and carotenoids, especially lutein and neoxanthin. Under high irradiance, LMA was greater and β-carotene (β-Car) and violaxanthin-cycle pool increased on a leaf area or Chl basis. The majority of plants contained α-Car in leaves, but the α- to β-Car ratio was always low in the sun, suggesting preference for β-Car in strong light. Shade and sun leaves had similar β,ε-carotenoid contents per unit Chl, whereas sun leaves had more β,β-carotenoids than shade leaves. Accumulation of Lx in leaves was found to be widely distributed among taxa: >5 mmol mol Chl-1 in 20% of all species examined and >10 mmol mol Chl-1 in 10% of woody species. In Virola elongata (Benth.) Warb, having substantial Lx in both leaf types, the Lx cycle was operating on a daily basis although Lx restoration in the dark was delayed compared with violaxanthin restoration.

High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations.

In view of anthropogenic global warming, heat tolerance of a neotropical pioneer tree, Ficus insipida Willd., was determined. Sections of sun leaves from a mature tree and from seedlings cultivated at ambient and elevated temperatures were heated to 42–53°C. Leaves from a late-successional tree species, Virola sebifera Aubl., were also studied. Widely used chlorophyll a fluorescence methods based on heat-induced rise of initial fluorescence emission, Fo, and decrease in the ratio of variable to maximum fluorescence, Fv/Fm, were reassessed. Fv/Fm determined 24 h after heat treatment was the fluorescence parameter most suitable to assess the lethal temperature causing permanent tissue damage. Thermo-tolerance was underestimated when Fo and Fv/Fm were recorded immediately after the heat treatment. The limit of thermo-tolerance was between 50 and 53°C, only a few °C above peak leaf temperatures measured in situ. The absence of seasonal changes in thermo-tolerance and only marginal increases in thermo-tolerance of plants grown under elevated temperatures suggest little capacity for further heat acclimation. Heat-stress experiments with intact potted seedlings also revealed irreversible leaf damage at 51–53°C, but plants survived and developed new leaves during post-culture.

Lutein epoxide cycle, light harvesting and photoprotection in species of the tropical tree genus Inga

Dynamics and possible function of the lutein epoxide (Lx) cycle, that is, the reversible conversion of Lx to lutein (L) in the light-harvesting antennae, were investigated in leaves of tropical tree species. Photosynthetic pigments were quantified in nine Inga species and species from three other genera. In Inga, Lx levels were high in shade leaves (mostly above 20 mmol mol(-1) chlorophyll) and low in sun leaves. In Virola surinamensis, both sun and shade leaves exhibited very high Lx contents (about 60 mmol mol(-1) chlorophyll). In Inga marginata grown under high irradiance, Lx slowly accumulated within several days upon transfer to deep shade. When shade leaves of I. marginata were briefly exposed to the sunlight, both violaxanthin and Lx were quickly de-epoxidized. Subsequently, overnight recovery occurred only for violaxanthin, not for Lx. In such leaves, containing reduced levels of Lx and increased levels of L, chlorophyll fluorescence induction showed significantly slower reduction of the photosystem II electron acceptor, Q(A), and faster formation as well as a higher level of non-photochemical quenching. The results indicate that slow Lx accumulation in Inga leaves may improve light harvesting under limiting light, while quick de-epoxidation of Lx to L in response to excess light may enhance photoprotection.

Sudden Exposure to Solar UV-B Radiation Reduces Net CO2 Uptake and Photosystem I Efficiency in Shade-Acclimated Tropical Tree Seedlings

Tree seedlings developing in the understory of the tropical forest have to endure short periods of high-light stress when tree-fall gaps are formed, and direct solar radiation, including substantial UV light, reaches the leaves. In experiments simulating the opening of a tree-fall gap, the response of photosynthesis in leaves of shade-acclimated seedlings (Anacardium excelsum,Virola surinamensis, and Calophyllum longifolium) to exposure to direct sunlight (for 20–50 min) was investigated in Panama (9°N). To assess the effects of solar UV-B radiation (280–320 nm), the sunlight was filtered through plastic films that selectively absorbed UV-B or transmitted the complete spectrum. The results document a strong inhibition of CO2assimilation by sun exposure. Light-limited and light-saturated rates of photosynthetic CO2 uptake by the leaves were affected, which apparently occurred independently of a simultaneous inhibition of potential photosystem (PS) II efficiency. The ambient UV-B light substantially contributed to these effects. The photochemical capacity of PSI, measured as absorbance change at 810 nm in saturating far-red light, was not significantly affected by sun exposure of the seedlings. However, a decrease in the efficiency of P700 photooxidation by far-red light was observed, which was strongly promoted by solar UV-B radiation. The decrease in PSI efficiency may result from enhanced charge recombination in the reaction center, which might represent an incipient inactivation of PSI, but contributes to thermal dissipation of excessive light energy and thereby to photoprotection.

Symbiotic vesicular-arbuscular mycorrhizae influence maximum rates of photosynthesis in tropical tree seedlings grown under elevated CO2

To investigate the importance of phosphorus and carbohydrate concentrations in influencing photosynthetic capacity of tropical forest tree seedlings under elevated CO2, we grew seedlings of Beilschmiedia pendula (Sw.) Hemsl. (Lauraceae) under elevated CO2 concentrations either with or without vesicular-arbuscular (VA) mycorrhizae. VA-mycorrhizae increased phosphorus concentrations in all plant organs (leaves, stems and roots). Maximum rates of photosynthesis (Amax) measured under saturating levels of CO2 and light were correlated with leaf phosphorus concentrations. VA-mycorrhizae also increased leaf carbohydrate concentrations, particularly under elevated CO2, but levels were low and within the range observed in naturally occurring forest species. Root carbohydrate concentrations were reduced in VA-mycorrhizal plants relative to non-mycorrhizal plants. These results indicate an important role for VA-mycorrhizae in controlling photosynthetic rates and sink strength in tropical trees, and thus in determining their response to future increases in atmospheric CO2 concentrations.

Growth irradiance effects on photosynthesis and growth in two CO-occurring shade-tolerant neotropical perennials of contrasting photosynthetic pathways

Dieffenbachia longispatha (C3) and Aechmea magdalenae (Crassulacean acid metabolism, CAM) are syntopic, neotropical forest perennials in central Panama that are restricted to shaded habitats. This is of particular interest for A. magdalenae because, like other understory CAM bromeliad species, it appears functionally and structurally to be better suited to life in full sun. Growth irradiance (GI) effects on photosynthesis and growth in both species were explored in the context of sun/shade trade-off concepts largely derived from studies of C3 plants. Potted plants were grown outdoors in 1, 55, and 100% full sun for 5 mo under well-watered conditions. While both species grew faster in high compared to low light, maximum relative growth rates (RGR) in full sun were still extremely slow with A. magdalenae showing a RGR approximately half that of D. longispatha. Photosynthetic capacity increased with GI in D. longispatha but not in A. magdalenae. Aechmea magdalenae responded to GI with shifts in the activity of the different CAM phases. Both species were photoinhibited in full sun, but more so in A. magdalenae. Despite possessing many traits considered adaptive in high light, these results suggest that A. magdalenae is unlikely to attain sufficient growth rates to thrive in productive, high-light habitats.

Effect of elevated CO2 and soil fertilization on whole-plant growth and water use in seedlings of a tropical pioneer tree, Ficus insipida Willd.

Summary Seedlings of the tropical pioneer tree species Ficus insipida were cultivated at present-ambient and elevated (about twice-ambient) CO 2 concentrations in open-top chambers located in a forest clearing near Panama City, Republic of Panama. To examine potential chamber-specific effects on growth and transpiration, plants were also studied outside chambers at ambient CO 2 levels. Plants were grown individually in 38 litre pots containing a mixture of soil and leaf litter, either in the absence or presence of a slow-release fertilizer. Data from three experiments, lasting 7 to 9 weeks each, are presented. Transpirational water loss of plants was determined gravimetrically. Fertilized plants grew more rapidly than unfertilized plants. Elevated CO 2 strongly enhanced biomass accumulation in fertilized plants. In unfertilized plants, elevated CO 2 enhanced growth in two experiments, but not in a third. Transpiration ratios (TR, g water lost: g dry mass accumulated) of plants grown in open-top chambers ranged from 176 (elevated CO 2 , plus fertilizer) to 336 (ambient CO 2 , minus fertilizer). The addition of fertilizer decreased TR by 15 to 20%, irrespective of the CO 2 concentration, and elevated CO 2 reduced TR by 27 to 35%, irrespective of whether fertilizer was present or not. The reduction in TR in response to elevated CO 2 was independent of whether biomass accumulation was enhanced by elevated CO 2 or not. In all experiments in which biomass accumulation was increased at elevated CO 2 , absolute water expenditure at elevated CO 2 was greater or similar to that at ambient levels – despite the lower TR at elevated CO 2 . In the single experiment in which elevated CO 2 did not lead to increased growth, the absolute water expenditure of plants was lower at elevated than at ambient CO 2 . There was no chamber effect on biomass accumulation, but TR of both fertilized and unfertilized plants was 19 to 31% higher inside compared to outside the open-top chambers.

Thermal tolerance, net CO2 exchange and growth of a tropical tree species, Ficus insipida, cultivated at elevated daytime and nighttime temperatures

Global warming and associated increases in the frequency and amplitude of extreme weather events, such as heat waves, may adversely affect tropical rainforest plants via significantly increased tissue temperatures. In this study, the response to two temperature regimes was assessed in seedlings of the neotropical pioneer tree species, Ficus insipida. Plants were cultivated in growth chambers at strongly elevated daytime temperature (39°C), combined with either close to natural (22°C) or elevated (32°C) nighttime temperatures. Under both growth regimes, the critical temperature for irreversible leaf damage, determined by changes in chlorophyll a fluorescence, was approximately 51°C. This is comparable to values found in F. insipida growing under natural ambient conditions and indicates a limited potential for heat tolerance acclimation of this tropical forest tree species. Yet, under high nighttime temperature, growth was strongly enhanced, accompanied by increased rates of net photosynthetic CO2 uptake and diminished temperature dependence of leaf-level dark respiration, consistent with thermal acclimation of these key physiological parameters.