Growth, photosynthesis and stress indicators in young rosewood plants (Aniba rosaeodora Ducke) under different light intensities

Crescimento, fotossíntese e indicadores de estresse em plantas jovens de pau-rosa (Aniba rosaeodora Ducke) sob diferentes intensidades luminosas

RESEARCH ARTICLE

Growth, photosynthesis and stress indicators in young rosewood plants (Aniba rosaeodora Ducke) under different light intensities

Crescimento, fotossíntese e indicadores de estresse em plantas jovens de pau-rosa (Aniba rosaeodora Ducke) sob diferentes intensidades luminosas

José Francisco de Carvalho Gonçalves^I, ^*; Denize Caranhas de Sousa Barreto^I; Ulysses Moreira dos Santos Junior^I; Andreia Varmes Fernandes^I; Paulo de Tarso Barbosa Sampaio^I; Marcos Silveira Buckeridge^II

^ILaboratório de Fisiologia e Bioquímica Vegetal, Instituto Nacional de Pesquisas da Amazônia, CP 478, 69011-970, Manaus, AM, Brasil

^IISeção de Fisiologia e Bioquímica de Plantas, Instituto de Botânica, CP 4005, 01061-970, São Paulo, SP, Brazil

ABSTRACT

Aniba rosaeodora is an Amazonian tree species that belongs to the family Lauraceae. Due to intense exploitation for extraction of essential oils (mainly linalol), A. rosaeodora is now considered an endangered species. On the other hand, there is little information about its ecophysiology which would be useful to support future forest planting programs. Hence, the effect of different light intensities on the growth and photosynthetic characteristics of young plants of A. rosaeodora was studied. Nine-month-old plants were subjected to four light treatments (T₁= 10 a 250 µmol.m^-2.s^-1 / control; T₂=500 to 800, T₃=700 to 1000 and T₄=1300 to 1800 µmol.m^-2.s^-1 / full sunlight). Allometric variables, gas exchange, contents of pigments and chlorophyll a fluorescence were analysed. As to the relative growth rates, it was found that plants of A. rosaeodora showed higher biomass accumulation when grown under intermediary irradiance conditions (T₂). The best photosynthetic performance was achieved under conditions of T₃. When growth was correlated with photosynthesis, it was found that plants under treatments T₂ and T₃ presented better responses in comparison with the lowest (T₁) and highest (T₄) light extremes. The highest pigment contents were obtained for plants in the shade (T₁) and the lowest for those exposed to full sunlight (T₄). The photochemical efficiency of photosystem II (F_v/F_m) was found that only plants in the shade treatment (T₁) presented no stress from high irradiance. These findings suggest that both treatments (T₁ and T₄) altered the function of the A. rosaeodora plants, inhibiting photosynthesis and growth. Plants of A. rosaeodora developed photo-protection mechanisms under full sunlight. However, the species presented better photosynthetic response and biomass gain under intermediary irradiance conditions, displaying relative physiological plasticity, during the seedling phase.

Key words: chlorophyll a fluorescence, chloroplast pigment contents, gas exchanges, photochemical efficiency of photosystem II, relative growth rate, tropical species.

RESUMO

Essa espécie arbórea da Amazônia, Aniba rosaeodora Ducke, pertence à família das Lauraceae. Em vista da intensa e desordenada exploração, visando à extração de óleos essenciais (linalol), o pau-rosa figura na lista de espécies ameaçadas de extinção. Poucos estudos ecofisiológicos têm sido feito no sentido de subsidiar futuros programas de plantios florestais. Dessa forma, pesquisou-se o efeito de diferentes irradiâncias sobre as características fotossintéticas e de crescimento em plantas de A. rosaeodora, na fase juvenil. Plantas com nove meses foram submetidas a quatro tratamentos de luz (T₁ = 10 a 250 µmol.m^-2.s^-1 / controle; T₂ = 500 a 800, T₃ = 700 a 1.000 e T₄ = 1.300 a 1.800 µmol.m^-2.s^-1 / pleno sol). Analisaram-se variáveis alométricas, trocas gasosas, teores de pigmentos cloroplastídicos e a fluorescência da clorofila a. Quanto ao crescimento relativo, observou-se que plantas de A. rosaeodora exibiram maior acúmulo de biomassa quando crescidas sob condições intermediárias de irradiância (T₂). O melhor desempenho fotossintético foi induzido por T₃. Quando se correlacionou crescimento com fotossíntese, percebeu-se que as plantas submetidas aos tratamentos T₂ e T₃ exibiram melhores respostas em comparação com os extremos de menor (T₁) e maior irradiâncias (T₄). Os maiores teores de pigmentos cloroplastídicos foram obtidos nas plantas sob sombra (T₁) e os menores teores encontrados naquelas expostas a pleno sol (T₄). Quanto à eficiência fotoquímica do fotossistema II (F_v/F_m) observou-se que apenas as plantas do tratamento de sombra (T₁) não apresentaram estresse por alta irradiância. Os resultados sugerem que ambos os tratamentos (T₁ e T₄) alteraram a funcionalidade das plantas de A. rosaeodora, inibindo a fotossíntese e o crescimento. A pleno sol, plantas de A. rosaeodora desenvolveram mecanismos de fotoproteção. No entanto, a espécie apresentou melhor resposta fotossintética e ganho de biomassa em condições intermediárias de irradiância, demonstrando relativa plasticidade fisiológica, durante o estádio juvenil.

Palavras-chave: eficiência fotoquímica do fotossistema II, espécies tropicais, fluorescência da clorofila a, pigmentos cloroplastídicos, taxa de crescimento relativo, trocas gasosas.

INTRODUCTION

The Amazon forest has suffered greatly due to the impacts of human activity (burning, deforestation and mining) and natural disturbances ("el niño" and "la niña", "blowdown" and tree falling). With regard to deforestation, recent estimates revealed that between 2001 and 2003 some 67,250 km² of Brazilian Amazonian forest have been cleared (INPE, 2004). One of the consequences is the decline of tree populations, especially of plant species that are used to produce extracts of commercial value. One example is rosewood (Aniba rosaeodora Ducke), a species of the family Lauraceae which is widely distributed throughout the tropical and subtropical regions of the planet (Werff and Richter, 1996). For decades, A. rosaeodora has been exploited for extraction of linalol, a product used in perfumes (Alencar and Fernandes, 1978). As a result, it is now believed that rosewood faces a serious risk of extinction (Rosa et al., 1997; May and Barata, 2004). Evidence of this decrease in the Amazonian populations of rosewood is the recent data of a reduction in the volume of linalol exported by the Amazonas state. In 1995 this state exported about 41 tons of linalol, whereas in 2000 the total volume produced decreased to 4 tons (Sampaio et al., 2003). One way to avoid the loss of populations of rosewood would be to prevent uncontrolled exploitation and at the same time to implement programs of reintroduction of this species in the ecosystem. However, the second measure is limited by the lack of information regarding the ecophysiology and forestry management of A. rosaeodora. These have been considered limiting factors in the implementation of large-scale plantation programs in the areas of extraction and natural management of the species. In this context, for rosewood plantations to be successful, it will be necessary to obtain more information about its ecophysiological strategies.

Among the main environmental factors, light is perhaps the most influential factor involved in the survival, growth and reproduction of tropical species. Light responses usually provoke physiological alterations, which are determinant for CO₂ assimilation and optimization of gas exchange (Sands, 1995). Light can also influence other physiological processes, both quantitatively and qualitatively. For this reason, environments that are either shaded or under full sunlight can inhibit the photosynthetic process, simply because there is too little or too much light (Zhang et al., 2003).

Indeed, it has been shown that the excess of light can affect plant growth and as a consequence provoke a reduction of field productivity as a result of photoinhibition (Kitao et al., 2000; Gonçalves et al., 2001; Marenco et al., 2001; Kull 2002). The different light intensities promote changes in both the physiology and morphology of the plants, which are features that result from the interaction between gene expression and the environment (Moraes Neto and Gonçalves, 2001). Normally, the measurement of the pigments from chloroplasts and the analysis of the fluorescence of chlorophyll a are used as stress indicators of high irradiance in the plants (Hendry and Prince, 1993; Stancato et al., 2001). The synthesis and/or degradation of chlorophyll occur naturally with the presence of light. Nonetheless, the excess of light can cause greater degradation and consequently, a reduction in the levels of total chlorophyll (Engel and Poggiani, 1991). In environments with high irradiance, the increase of photooxidation of chlorophyll depends upon the concentration of carotenoids, which can prevent photoxidative action (Bartley and Scolnik, 1995). Additionally, the excess of irradiance can contribute to the decrease of photosynthetic capacity which in turn contributes to the occurrence of photoinhibition (Kitao et al., 2000). Photoinhibition is triggered by inactivation of the photochemical reaction centre in photosystem II, probably as a result of damage suffered by the D1 protein (Krause et al., 1999) which under conditions of high irradiance can become inactivated or even undergo irreparable degradation, thus jeopardizing the photosynthetic mechanism (Baker and Bowyer, 1994).

An efficient photosynthetic activity is necessary for high production of plant biomass. Nevertheless, abiotic factors (light, water, CO₂ and nutrients) and physiologically controlled factors (stomatic conductance, transpiration) can strongly influence this activity. In the present study, we followed growth, gas exchange, pigment concentrations and photochemical efficiency of photosystem II in young plants of A. rosaeodora subjected to increasing levels of irradiance.

MATERIAL AND METHODS

Study area and experiment installation: The study was conducted under nylon tarpaulins at the National Institute of Amazonian Research in the V-8 campus in Manaus, Amazonas, Brazil. According to Koppen's climatic classification, the climate of this region is of the Afi type with an average annual precipitation of 2200 mm and average temperature of 27 ± 5 ºC. The experiment was installed using 9-month-old rosewood (Aniba rosaeodora Ducke) plants produced from seeds collected from Adolpho Ducke Forest Reservation, located at Km 25 of the AM-10 highway (Manaus-Itacoatiara). Healthy seeds were selected following a model of uniformity in size. After soaking in 1 % (v/v) sodium hypochlorite solution for 10 min and thoroughly washed with tap water. The seeds were then placed in plastic boxes containing washed sand for germination. Once the plants reached 10 cm in height, they were transplanted to black polyethylene bags containing 5 kg of compost mixture and sand (2:1, w/w), where they remained for 25 days for an acclimation period. Plants were then subjected to 4 different levels of light intensities: T₁ = 10 to 250 for control treatment, under plant cover; T₂ = 500 to 800 obtained with nylon cover; T₃ = 700 to 1000 obtained with nylon cover; T₄ = 1300 to 1800 µmol.m^-2.s^-1 obtained by leaving plants under direct sunlight. During the experiment, plants were watered daily.

Growth analysis: The growth of the rosewood plants was evaluated by allometric readings and mass determination. The relative growth rates of different plant parts such as leaves, stem and roots were obtained while measurements were made at the beginning and end of the experiment. The measurements were taken at the beginning and end of a six month period (180 days). Upon completion of the experiment, leaves, stems and roots were separated and oven-dried at 70ºC until the dry material reached constant mass. The determination of the relative growth rate of the leaf (RGR-L), stem (RGR-S), root (RGR-R) and total (RGR-Total) biomass was achieved using the equations below according to the methodology described by Bugbee (1996) and Davanso et al. (2002):

The variables are represented by L₁ = initial leaf mass (g), L₂ = final leaf mass (g), S₁ = initial stem mass (g), S₂ = final stem mass (g), R₁ = initial root mass (g), R₂ = final root mass (g), t₁ = initial time (months) and t₂ = final time (months).

Gas exchange measurements: Photosynthesis (A_max), dark respiration (R_d), stomatic conductance (g_s) and transpiration (E) were determined with a portable, open system, infrared gas analyser (IRGA), model LI-COR 6400. The measurements were made between 20 and 30 days after the installation of the experiment. In addition, the measurements were made between 9:00 and 11:00 a.m. on completely expanded leaves located in the middle-third of the plant. Five replicates of each measurement were obtained. Light curves were made for a photon flux density (PPFD) between 0 and 2000 µmol.m^-2.s^-1 and the leaf chamber equipment was adjusted to analyse concentrations of CO₂ and water vapour at 385±10 µmol.mol^-1 and 21 ± 1 mmol.mol^-1, respectively, with a temperature of 31 ± 1ºC. For data analysis, the model of the non-rectangular hyperbole equation was used to adjust the photosynthetic response to light curve for each plant (Lieth and Reynolds, 1987):

where A represents the rate of net photosynthesis [ìmol CO₂.m^-2.s^-1], A'_maxrepresents the rate of maximum photosynthesis under conditions of saturated light, f_a represents the apparent quantum yield [mol CO₂.mol^-1 (quanta)], I represents the light intensity, and Q represents the regression curve factor. In order to avoid a correlation between f_a and Q, during the curve adjustment, f_a was first estimated using a linear regression from the initial portion of the curve between 0 and 100 µmol.m^-2.s^-1, using f_a as the angular coefficient of the linear regression. The values of A'_max and Q were estimated with a non-rectangular hyperbole regression described by Lieth and Reynolds (1987) and using the software Statistics 6.0 Windows version (StatSoft, Inc., Tulsa, USA). The value of A_maxwas estimated from the curve adjustment, corresponding to the value of A at the PPFD point equal to 2000 µmol.m^-2.s^-1. The light compensation point (I_c; PPFD in which A = 0) was calculated by the formula I_c = R_d / f_a and the light saturation (I_s; PPFD in which A = 90% A_max) was estimated by the equation (5).

The water-use efficiency (WUE) and the intrinsic water-use efficiency (WIUE) were calculated using the following equations [mmol CO₂.mol^-1(H₂O)] = photosynthesis (A) / transpiration and IWUE [µmol CO₂.mol^-1 H₂O ] = photosynthesis / stomatal conductance.

Pigment analysis: After the gas exchange readings, the marked leaves were collected for pigment analysis. These were performed with 0.1 g of fresh material ground in 10 mL of 80 % acetone and magnesium carbonate (MgCO₃) and immediately afterwards 10 mL of 100 % acetone were added. The suspension was filtered and absorbance was read at 663 nm (chlorophyll a – Chl a), 645 nm (chlorophyll b – Chl b) and 480 nm (carotenoids – C_x+c) (Hendry and Price, 1993)

Chlorophyll a fluorescence measurements: The chlorophyll fluorescence was determined using a portable fluorometer (Plant Efficiency Analyser-PEA, MK2-9600-Hansatech, Norfolk, UK) between 9:00 and 11:00 am on leaves located in the middle-third of the plant. For each treatment, five leaves were selected (subsamples) as replicates. The leaves of A. rosaeodora were subjected to a period of dark adaptation for 15 min. Leaves were then exposed to a pulse of high intensity saturated light (2250 µmol m^-2 s^-1) and the fluorescence measurements were taken immediately afterwards (Gonçalves et al., 2001). From the induction of fluorescence of fast kinetics, the initial fluorescence (F_o), maximum fluorescence (F_m), variable fluorescence (F_v = F_m – F_o) and photochemical efficiency of PSII (F_v/F_m) were obtained. The measurements were made in three periods of evaluation: 2, 30 and 60 days after the installation of the experiment.

Experimental design and statistical analysis: The experimental design was completely randomised with 4 treatments and 5 replicates. The data was subjected to variance analysis and the means were compared by the Tukey test at 5 % probability. In addition, regression analyses were applied for the light curve adjustments. The software Statistics (version 6.0) and SAEG/UFV (version 5.0) were used for statistical analysis.

RESULTS AND DISCUSSION

Young plants of A. rosaeodora subjected to the 500 to 800 µmol.m^-2.s^-1 (treatment T₂) exhibited higher values for the relative growth rates of leaf (RGR-L), stem (RGR-S), root (RGR-R) and total mass (RGR-total) when compared with high light intensity treatment T₄ (1300 to 1800 µmol.m^-2.s^-1, Figure 1). For treatment T₄, there was a loss of leaf mass of the plants (-0.005 g.g^-1.m^-1). In addition, plants in T₂ presented values of RGR-S, RGR-R and RGR-total approximately 50, 225 and 67 % greater than the values found for treatment T₁ and 125, 550 and 650 % greater than the values found for treatment T₄, respectively (figure 1).The response of most trees to changes in light intensity varies depending on the species (Thompson et al., 1992). Some studies revealed that plants growing under shade exhibit a lower biomass production when compared with plants growing under higher irradiance (Huante and Rinc, 1998; Nakazono et al., 2001). Nevertheless, when some species are subjected to conditions of high light intensity, they may show a decrease in the accumulation of biomass due to photoinhibition (Stancato et al., 2002). In the case of A. rosaeodora, our results indicate that conditions corresponding to treatment T₂ (500 to 800 µmol.m^-2.s^-1) improved performance of the plants. This can be seen by the higher accumulation of biomass in the roots and shoots of the plant (figure 1).

The maximal photosynthetic rates (A_max) ranged from 2.27 to 6.92 µmol CO₂.m^-2.s^-1 among treatments, with a range of 205 % from the lowest to the highest values (table 1). The plants in T₃ (700 to 1000 µmol.m^-2.s^-1) showed the greatest rate of photosynthesis while the plants in T₄ (1300 to 1800 µmol.m^-2.s^-1) exhibited the lowest values of A_max (table 1 and figure 2). It was also observed that the highest value of A_max found for A. rosaeodora ranges among values found for other tropical tree species that varied between 2.2 and 18.2 µmol.m^-2.s^-1 (Zotz and Winter, 1994; Barker et al., 1997; Loik and Holl, 2001; Marenco et al., 2001; Santos and Buckeridge, 2004). Although these responses can be determined by the age of the plant, time of year and ecological function (pioneer, intermediate or climax), light intensity has been considered one of the most important factors that affect the functioning of the photosynthetic mechanism and the adaptation to the light conditions in the environment (Pessarakli, 1997). For A. rosaeodora, the relatively low photosynthetic efficiency exhibited by treatment T₄ resulted in lower investment in biomass, which may be associated with stress due to high light intensity. Dark respiration (R_d) ranged from 0.61 to 1.16 µmol CO₂.m^-2.s^-1, in which the values increased with increasing light intensity (table 1). It is also important to point out that R_d is of great use for the production of the energy necessary for plant growth according to Lambers et al. (1998). The rates of R_d are influenced by environmental factors, exhibiting higher rates under conditions of high irradiance. With regard to the apparent quantum yield (f_a), we observed that treatment T₂ had the highest value (0.037 mol CO₂.mol^-1 photons) whereas T₃ and T₁ were intermediate and T₄ (0.021) showed the lowest value (table 1). The low value found for T₄ could be associated with an excess of light. Marenco et al. (2001), in a study of the species Swietenia macrophylla, found the highest values for f_a in environments with direct sunlight exposure. This finding may be related to the influence of different environmental conditions and the intrinsic characteristics of each species, since some species may possess either greater or lower photosynthetic plasticity. For the convexity factor (Q), the values ranged from 0.92 to 0.97 (table 1). Considering that the convexity factor is related to light saturation in the chloroplasts, this variable could change in the presence of high irradiance. The values of Q decreased in response to the increase in light in treatments T₁ to T₃, indicating more efficient response to the use of light energy at intermediate levels of irradiance. However, a high value for Q in the treatment exposed to direct sunlight (T₄) could reflect the degree of photoinhibition resulting from high light intensity (Werner et al., 2001).

Plants under conditions that potentially lead to photoinhibition tend to exhibit a decrease in photosynthesis and generally result in an increase in Q as observed in the plants subjected to treatment T₄. With regard to the compensation irradiance (I_c), the values ranged from 19 to 54 umol.m^-2.s^-1 and increased with increasing light intensity. The highest value of I_c found for A. rosaeodora in the treatment exposed to direct sunlight (T₄) was a result of the high value of R_d and the low value of f_a. Light saturation (I_s) for A. rosaeodora showed a positive response to the increasing light intensities for the first three treatments (T₁, T₂ and T₃), but a reduced response when subjected to direct sunlight, which may be indicative of photosynthetic damage resulting from excess light (Werner et al., 2001).

It is well known that light saturation varies in function of light intensity and the species being examined. In A. rosaeodora, it was observed that I_s as well as I_c increase with increasing light intensities in the first three treatments (T₁, T₂ and T₃). This was also observed in treatment T₄, where there was a decrease in I_s (table 1). These results suggest that under high light intensity, damage caused by photoinhibition of the photosynthetic apparatus may have inhibited the ability of the system to cope with an excess of electrons in the photochemical processes. This also resulted in high values of Q. Different values of light saturation have been found for many species in different environmental conditions (Chow et al., 1998; Krause et al., 1999; Marenco et al., 2001; Aidar et al., 2002; Santos and Buckeridge, 2004). Additionally, under some microenvironmental conditions the photosynthetically active radiation varies both spatially and temporally, thus inducing plants to develop mechanisms of acclimation and greater plasticity to face different conditions of light (Zhang et al., 2002). This appears to be the case in certain regions of the Amazon forest. Data collected in one of the towers installed near Manaus (ZF-2) shows that the maximal light intensity near the ground of the forest, can reach rather high values such as 1000 µmol.m^-2.s^-1 for several consecutive days. This period can be preceded and subsequently followed by short periods of lower light intensities ranging from 200 to 300 µmol.m^-2.s^-1. Thus, plants must be able to respond to light in a rather flexible manner so that they can survive in the understorey of the rain forest. This probably explains the observed changes in the saturation points when all variables associated with photosynthesis change (table 1 and figure 2).

Regarding water use efficiency (WUE), it was observed that when young plants of A. rosaeodora grew under direct sunlight (T₄) a lower transpiration rate (E) was observed (table 2). This indicates that this species presents a relatively low WUE when subjected to high light intensity. Stomatic conductance (g_s), ranged from 116 to 174 mmol.m^-2.s^-1. These values are between those found for other tropical species, which vary between 97 and 1250 mmol.m^-2.s^-1 (Jarvis and McNaughton, 1986; Carswell et al., 2000; Loik and Holl, 2001; Marenco et al., 2001). Therefore, the values of g_s in A. rosaeodora are low and might be related to ecophysiological features of the species in respect to its ecological function (mid - successional).

Water use efficiency ranged from 1.08 to 2.79 mmol CO₂.mol^-1 H₂O, and a higher value was observed in treatment T₃ than in treatment T₄ (table 2). For the intrinsic water use efficiency (IWUE), the highest value (45 mmol CO₂.mol^-1 H₂O) was also observed in treatment T₃ (table 2). These results indicate that A. rosaeodora exhibit limitations in relation to the use of water as a result of the partial opening of the stomata, with a decrease in the values of IWUE due to the increase in light intensity.

Pigment concentrations (Chl a, Chl b, Chl_total and C_x+c) for the treatment in the shade (T₁) were respectively176, 159, 174 and 83 % greater than the concentrations found for the treatment in direct sunlight (T₄) (table 3). It was also observed that the levels chlorophylls a and b tended to decrease with the increase in light intensity (table 3). Similar results were found by Nakazono et al. (2001). The synthesis and degradation of the photosynthetic pigments are normally associated with the photosynthetic efficiency of the plants as well as their growth and adaptability to different environments (Engel and Poggiani, 1991). The chlorophylls are usually synthesized and photo-oxidised in the presence of light (Kramer and Kozlowski, 1979). However, under conditions of high light intensity, the degradation of the chlorophyll molecules might be more intense and equilibrium occurs at lower concentrations.

It was observed that the chlorophyll concentrations in shaded leaves tend to be higher when compared with leaves exposed to direct sunlight (Boardman, 1977). Under field conditions in Central Amazonia, adult plants of Swietenia macrophylla and Dipteryx odorata exhibited similar behaviour, in which the concentrations of pigments in leaves of plants under shade treatment were greater than the concentration of those exposed to direct sunlight (Gonçalves et al., 2001).

Regarding the ratio between chlorophylls (Chl a/b), no differences amongst the species studied were found. According to Whatley and Whatley (1982), a greater proportion of chlorophyll b in leaves of shaded plants is an important characteristic because it allows for the capture of energy at different portion of the electromagnetic spectrum. Krause et al. (2001) observed differential responses in the values of Chl a/b for plants of Dryepetes standleyi growing in small, medium, and wide gaps in the forest. D. standleyi exhibited the lower levels of chlorophyll when growing in medium gaps whereas Quararibea asterolepsis exhibited the lowest levels in wide gaps. The behaviour of Q. asterolepsis is similar to that shown here for A. rosaeodora.

In A. resaeodora the ratios total chlorophyll /carotenoids (Chl_total/C_x+c) ranged from 2.0 to 3.0 among treatments. Plants subjected to treatment T₁ had the highest value and the plants subjected to treatment T₄ had the lowest. The lowest value for Chl_total/C_x+c in treatment T₄ may be considered as a photoprotective mechanism against high irradiance. These results suggest that A. rosaeodora, usually classified as a mid-successional species, showed considerable plasticity for capture and usage of light, particularly at young stages, by increasing the concentration of pigments under low light conditions and decreasing Chl_total/C_x+c at high irradiance to minimize the damage caused by photoinhibition.

Regarding chlorophyll a fluorescence, it was observed that the initial fluorescence (F_o) did not vary significantly among the treatments with the exception of the treatment in direct sunlight, which after 30 days presented a decrease in the initial fluorescence followed by an increase after 60 days (figure 3A). Similar behaviour was observed over the different periods, in which the treatments T₂, T₃ and T₄ experienced a decrease in both F_v and F_m after 30 days, before returning to their normal values (figures 3B and 3C, respectively).

For the photochemical efficiency of PS II (F_v/F_m = (F_m-F_o)/F_m), the shaded treatment induced stability in its behaviour over the experimental period. In the treatments T₂ and T₃, the plants showed a decrease in F_v/F_m after 30 days, and subsequently returned to normal behaviour after 60 days. In the treatment where plants were exposed to direct sunlight (T₄), strong photoinhibition was observed (figure 3D). It is possible that the increase in temperature might have contributed to photoinhibition (Kitao et al., 2000). On the other hand, Gonçalves et al. (2001) observed for S. macrophylla (mid-successional species) a decrease of 6% in F_v/F_m whereas for D. odorata (late-successional) no differences were observed between plants grown under high and low light intensities. It is possible that the small difference observed for the former species could be related to mechanisms of adaptation of mid-successional species to higher light intensities. Such a behaviour was observed for A. rosaeodora, whose F_v/F_m ratio decreased along the 60 days of the experiment.

Zhang et al. (2002) observed significant decrease in F_v/F_m in saplings grown under low light density and suddenly exposed to high light intensity, indicating that photosystem II was partially inactivated. Krause et al. (2001) observed that during the periods of direct sun exposure, all the plants exhibited significant photoinhibition of PS II as revealed by a decrease in F_v/F_m.

Indeed, exposition to excess of light may cause photoinhibition to a degree that is dependent on the species. This can be measured by the decrease in the parameter of the fluorescence of chlorophyll a (F_v/F_m), after exposure to light, representing the maximum photochemical efficiency of photosystem II (Werner et al., 2001). When A. rosaeodora was subjected to treatment T₄, we observed a steady decrease in F_v/F_m, which characterised a high level of photoinhibition. The reduction of F_v/F_m could be the result of an increase in F_o or a decrease in F_m (Kitao et al., 2000; Oliveira et al., 2002). Nonetheless, after 30 days and 60 days, there was an increase in the values of F_v/F_m, indicating that there had been an effective response to stress involving an acclimation mechanism to high irradiance. Thus, A. rosaeodora was able to adjust its photosynthetic apparatus when subjected to different conditions of light during growth. The consequence of photoinhibition seems to be confirmed by the observations of low values of photosynthesis (measured between 20 and 30 days after the installation of experiment) and biomass accumulation found in plants of A. rosaeodora subjected to direct sunlight.

The process of acclimation to environments of high irradiance is rather complex, involving the availability of both water and nutrients. In this study, the physiological behaviour of young plants of A. rosaeodora subjected to different light intensities, suggests that its photosynthetic apparatus is more efficient when subjected to environments of medium light intensity, between 500 a 1000 µmol.m^-2.s^-1. On the other hand, our results show that the photosynthetic activity of this species may be limited when grown in shaded environments or environments with high light intensity, either due to insufficient light intensity in the shaded environment (T₁) or to photoinhibition as a consequence of the excess light in the open environment (T₄). The better photosynthetic performance of the species resulted in a greater ability to accumulate biomass. Regarding photosynthetic pigments, we observed that A. rosaeodora exhibited plasticity in light capture, developing a photoprotective mechanism when subjected to high intensities of irradiance. Furthermore, A. rosaeodora exhibited a higher photosynthetic performance and consequently a higher capacity of biomass accumulation under intermediate light intensities (between 500 a 1300 ìmol photons.m^-2.s^-1). On the other hand, extremes of light intensity can limit photosynthesis of young plants of A. rosaeodora. Thus, these results indicate that intermediate light conditions are the more adequate for this species to reach higher levels of carbon assimilation and biomass accumulation during its early growth phase.

Received: 03/08/2005, Accepted: 03/10/2005

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Publication Dates

• Publication in this collection
  22 Nov 2005
• Date of issue
  Sept 2005

History

• Accepted
  03 Oct 2005
• Received
  03 Aug 2005