Photosynthetic traits of five neotropical rainforest tree species: interactions between light response curves and leaf-to-air vapour pressure deficit

BIOLOGICAL AND APPLIED SCIENCES

Photosynthetic traits of five neotropical rainforest tree species: interactions between light response curves and leaf-to-air vapour pressure deficit

Marcelo Schramm Mielke^*; Alex-Alan Furtado de Almeida; Fábio Pinto Gomes

Departamento de Ciências Biológicas; Universidade Estadual de Santa Cruz (DCB/UESC); Rodovia Ilhéus-Itabuna, km16; 45650-000; [e-mail]; Ilhéus - BA - Brasil

ABSTRACT

Measurements of leaf gas exchange at different photosynthetic photon flux density (PPFD) levels were conducted in order to compare the photosynthetic traits of five neotropical rainforest tree species, with a special emphasis on empirical mathematical models to estimate the light response curve parameters incorporating the effects of leaf-to-air vapour pressure deficit (D) on the saturated photosynthetic rate (A_max). All empirical mathematical models seemed to provide a good estimation of the light response parameters. Comparisons of the leaf photosynthetic traits between different species needed to select an appropriate model and indicated the microenvironmental conditions when the data were collected. When the vapour pressure deficit inside the chamber was not controlled, the incorporation of linear or exponencial functions that explained the effects of D on leaf gas exchange, was a very good method to enhance the performance of the models.

Key words: Brazilian atlantic rainforest; ecosystem process models; net photosynthetic rate

RESUMO

Medições das trocas gasosas foliares em diferentes níveis do densidade de fluxo de fótons fotossintéticamente ativos (PPFD) foram realizadas com o objetivo de comparar as características fotossintéticas de cinco espécies arbóreas de florestas úmidas neotropicais, com especial ênfase em modelos matemáticos empíricos para estimativa de parâmetros derivados das curvas de resposta à radiação luminosa e dos efeitos da diferença de pressão de vapor entre a folha e o ar (D) na taxa fotossintética em saturação luminosa (A_max). Os modelos analisados proporcionaram boas estimativas para os parâmetros derivados das curvas de resposta à radiação luminosa. Comparações entre as características fotossintéticas de diferentes espécies devem sempre considerar os modelos utilizados, seguidas de indicações pormenorizadas das condições microambientais no momento em que os dados foram coletados. Quando a diferença de pressão de vapor não for controlada artificialmente durante as medições, a incorporação de uma função linear ou exponencial, explicando os efeitos de D nos parâmetros de trocas gasosas, é um excelente método para incrementar a performance dos modelos.

INTRODUCTION

Tropical rainforests represent a great proportion of the terrestrial biomass productivity (Malhi and Grace, 2000) and studies that evaluate leaf photosynthetic characteristcs of tree species are needed to quantify the carbon dynamics at regional and global scales. Knowledge of leaf photosynthetic traits is needed to understand the carbon cycles of a particular forest ecosystem, to evaluate theoretical aspects of ecological succession, to select intercrop species in agroforestry (Bazzaz and Pickett, 1980; Barker et al., 1997; Lüttige, 1997), and to parameterize ecosystem process models that are used as tools for the assessment of sustainable yields from natural and planted forests, or to estimate the total net primary productivity as the stand grows (Running and Coughan, 1988; McMurtrie, 1993; Aber et al., 1996; Landsberg and Gower, 1997).

It is well established that photosynthesis responds to light or photosynthetic photon flux density (PPFD), expressed as the moles of photons between 400-700 nm per square meter per second in a non-linear mathematical function (Nobel, 1991). Different empirical (Thornley, 1976; Leverenz, 1994; Ögren and Evans, 1993) and mechanistic models (Farquhar et al., 1980; Farquhar and von Caemmerer, 1982) to estimate photosynthesis have been proposed and discussed in the literature. Despite some differences between the formulas, all these models were ultimately proposed with the same objective, i.e. to estimate photosynthetic light response parameters, such as the light saturated photosynthetic rate (A_max) and the apparent quantum yield (a) that explained the responses of photosynthesis to environmental variables and permited modelling leaf to canopy carbon exchange (Beyshlag and Ryel, 1998). Despite of the high accuracy of the mechanistic models, empirical mathematical models have the advantage that they are easily parameterized from the data collected in field conditions. Empirical models are currently used and the derived parameters have been presented and discussed in several studies about different aspects of tree and forest ecophysiology (Prado et al., 1994; Kubiske and Pregitzer, 1996; Sullivan et al., 1996; Kitajima et al., 1997; Valladares et al., 1997; Eschenbach et al., 1998; Evans et al., 2000; Hiremath, 2000). However, there are no reports on the forest ecophysiology comparing these models and the associated light response curve parameters.

Other environmental factors also affect the net photosynthetic rate such as air temperature, atmospheric CO₂ molar fraction and vapour pressure deficit (Nygren, 1995; Pachepsky and Acock, 1996; Day, 2000). In tropical rainforests, vapour pressure deficit changes at temporal and spatial scales (Lüttige, 1997). Because the vapour pressure deficit is directly dependent on relative humidity and air temperature (Landsberg, 1986), this microenvironmental factor is highly variable during the day or between days (Granier et al., 1996; Ishida et al., 1996) and depends on growth environmental conditions, such as forest gaps, abandoned agricultural lands or forest understory (Barker et al., 1997; Loik and Holl, 2001). High vapour pressure deficit values can induce stomatal closure and limits the influx of CO₂, with a strongly effect on the diffusive phase of photosynthesis. For many tropical and temperate tree species, the closing of the stomata has been observed as a function of the increases in the evaporative demand of the atmosphere (Dolman and Van Den Burg, 1988; McCaughey and Iacobelli, 1993; Landsberg and Gower, 1997; Yang et al., 1998; Mielke et al., 1999). Also, the sensitivity of the stomata to the vapour pressure deficit is largely variable between different plant species (Franks and Farquhar, 1999).

The aim of this study was to compare the photosynthetic traits of five neotropical rainforest tree species with a special emphasis on the use of empirical models to estimate light response curve parameters and the effects of the leaf-to-air vapour pressure deficit on the light saturated photosynthetic rates (A_max).

METHODS

The measurements were performed in the arboretum of the Universidade Estadual de Santa Cruz (UESC) and at the Centro de Pesquisas do Cacau (CEPEC)/CEPLAC, both located in the county of Ilhéus (14º47'S, 39º10'W, 15 masl), and at the Estação Experimental Lemos Maia (ESMAI)/CEPLAC, located in the county of Una (15º15'S, 39º05'W, 105 masl), Bahia, Brazil. The studied species were Caesalpinia peltophoroides Benth. (Caesalpinaceae), Macrolobium latifolium Vog. (Caesalpinaceae), Manilkara salzmannii (DC.) Lamb. (Sapotaceae), Theobroma cacao L. (Sterculiaceae) and Theobroma grandiflorum (Wild. ex Spring) Schumann (Sterculiaceae). The first three species were grown in the UESC's arboretum, while T. cacao was grown in a shade house in the nursery of CEPEC/CEPLAC and T. grandiflorum in an agroforestry system, partially shaded by a Cocos nucifera L. plantation, in ESMAI/CEPLAC. Among the species studied, C. peltophoroides, M. latifolium and M. salzmannii were native to the southern Bahian atlantic rainforest and have been very important, both economically and ecologically. C. peltophoroides and M. latifolium are fast-growing secondary species that naturally grows at moderate shade to full sunlight, and M. salzmannii is a slow-growing late successional species. T. cacao and T. grandiflorum are shade tolerants late secondary species. These species are native to the Amazon basin, being cultivated in agroforestry systems.

Leaf gas exchange was measured in one single mature and completely expanded leaf of several individuals per species, always between 930-1330. Light response curves were obtained using a Portable Photosynthesis System LI-6400 (Li-Cor, USA), equipped with an artificial light source 6400-02B RedBlue. Leaf gas exchange measurements at different levels of photosynthetic photon flux density incident at leaf surface (PPFD) were made using the "Light curve" routine of the Open 3.3 software (Li-Cor, USA). Measurements were taken at eight levels of PPFD, i.e. 0, 50, 100, 200, 400, 800, 1200 and 1600 µmol photons m^-2 s^-1 for the species growing at arboretum conditions (C. peltophoroides, M. latifolium and M. salzmannii) and at seven levels of PPFD, i.e. 0, 50, 100, 200, 400, 800 and 1200 µmol photons m^-2 s^-1 for the species growing in shaded and partially shaded environments (T. cacao and T. grandiflorum). The measurements were always performed from the upper to the lower values of PPFD. The minimum time allowed for the reading stabilization at each level of PPFD was 120s, and the maximum time for saving each reading was 150s. The maximum coefficient of variation allowed for each reading's save was set to 1%. Seven to nineteen light response curves per species were obtained, depending on the species and sites: C. peltophoroides (n = 7), M. latifolium (n = 10), M. salzmannii (n = 10), T. cacao (n = 7) and T. grandiflorum (n = 19).

The net photosynthetic rate by unit of leaf area (A) and the stomatal conductance to water vapour (gs) were calculated, respectively, using the values of CO₂ and humidity variation inside the chamber, both measured by the infrared gas analyzer of the portable photosynthesis system. Dark respiration (Rd) corresponded to readings of PPFD = 0 µmol photons m^-2 s^-1. With the exception of PPFD, no microenvironmental variable inside the chamber was controlled. Values of atmospheric CO₂ molar fraction (Ca), leaf (T_L) and air temperature inside the chamber (T_A) were obtained from the sensors of the equipment, while leaf-to-air vapour pressure deficit (D) and intercelullar air space CO₂ molar fraction (Ci) were estimated by the Open 3.3 software. The ratios of intercelullar to atmospheric CO₂ molar fractions were calculated by dividing Ci by Ca.

To estimate photosynthetic light response parameters a simple rectangular hiperbola, described by Thornley (1976) and Landsberg (1986), was rewritten and used in the form:

A=A_max[PPFD/(b+PPFD)]-Rd (Model 1)

were A is the net photosysthetic rate, A_max is the light saturated photosynthetic rate, b is the point of inflexion of the curve, which was defined as one half of the saturated PPFD, and Rd is the dark respiration rate. Three variations of this model were tested, incorporating mathematical functions that explain the effects of D on A_max:

A=A_max[PPFD/(b+PPFD)](1-D/g)-Rd (Model 2)

A=A_max[PPFD/(b+PPFD)]exp(-gD)-Rd (Model 3)

A=A_max[PPFD/(b+PPFD)](D^-g)-Rd (Model 4)

were g is a coefficient that indicates the sensitivity of leaf gas exchange to D.

A Gauss-Newton non-linear estimate routine of Statistica for Windows, version 5.0 (StatSoft, 1995) was used to obtain the best fittings for all the models. After this procedure, the values of A_max from the models 2, 3 and 4 were corrected based on the mean value of D observed in all of the measurements (1.70 ± 0.02 kPa, n = 388). In all models, the values of the apparent quantum yield (a) were estimated as: a = A_max/b.

The results were interpreted and discussed based on the different light response curve parameters estimated from the models and species environmental growth conditions. Simple statistical comparisons between the models were made by comparing the values of regression coefficients (r²) and the graphical analysis. Residual analysis were also conducted in order to interpret the effects of D on the values of A estimated from the different models.

RESULTS

Measurements of leaf gas exchange made at different days and environmental conditions generated differences in the microenvironmental variables inside the chamber (Table 1). The maximum mean values of D and T_A were observed for T. grandiflorum, whereas the minimum values of these variables were observed for C. peltophoroides. The mean values of Ca varied from 373.6 to 380.1 µmol mol^-1, for C. peltophoroides and M. latifolium, respectively. The average maximum values of the saturated net photosynthetic rate, measured at 1600 µmol photons m^-2 s^-1 for C. peltophoroides, M. latifolium and M. salzmannii and at 1200 µmol photons m^-2 s^-1 for T.cacao and T. grandiflorum, were observed in the species that were growing in arboretum conditions. The maximum and minimum mean values of A_sat were observed for C. peltophoroides and T. cacao (10.51 and 5.69 µmol CO₂ m^-2 s^-1, respectively). Similarly, the maximum and minimum values of stomatal conductance measured simultaneously with A_sat (gs_sat) were also observed for these two species (0.238 mol H₂O m^-2 s^-1 for C. peltophoroides, and 0.086 mol H₂O m^-2 s^-1 for T. cacao). The maximum values of the Ci/Ca ratio were also observed in C. peltophoroides (0.72) and the minimum values were observed in T. grandiflorum (0.61).

Based on all species, strong effects of D on A_sat and gs_sat were observed, in which the linear and exponential functions provided the highest values of r² (Fig. 1). Direct relationship was also observed between gs_sat and A_sat (Fig. 2), indicating a strong dependence of the saturated net photosynthetic rates to stomatal conductance.

The best fittings for Model 1 were observed for M. latifolium (Table 2). When the growth conditions of the species were compared, large differences between the statistical parameters were observed, but when the models were compared within the same species, little differences were observed for the regression coefficients (r²).

Differences between the values of light response curve parameters were also observed. For all the species, the very best fittings were obtained with Models 2 and 3, in which the smallest value of r² was observed in M. salzmanii (0.75). The fitted data based on Model 3 and the measured values are presented in Fig. 3.

The smallest differences between measured and estimated values of A, in all classes of D (Table 3) were observed in models in which the microenvironmental parameter was included. Model 1, on the other hand, had a tendency to underestimate A at low D and overestimate A at high D (i.e. below and above 1.5 and 3.0 kPa, respectively). The highest mean values of the residuals were also observed for the Model 1, above 2.5 kPa.

All models provided good estimates of Rd (Table 4), but a poor relationship between measured and estimated values of A_sat was observed for the Model 1. In this case, the best results were observed in Models 2 and 3, in which linear or exponencial functions that explained the effects of the leaf-to-air vapour pressure deficit on leaf gas exchange, were incorporated.

DISCUSSION

The observation of the highest values of A_sat and gs_sat in trees growing at arboretum conditions was expected because the leaves of these trees were constantly exposed to full sunlight and all were canopy trees; moreover, the environmental conditions, especially light and atmospheric CO₂, have strong influences on the leaf gas exchange characteristics of the leaves (Kubiske and Pregitzer, 1996; Sullivan et al., 1996; Evans, 2000). The average maximum values of A measured in this study were similar to those of other neotropical forest tree species in field conditions, for instance the values measured by Hogan et al. (1995) in leaves of Anacardium excelsum (8.62), Cecropia longipes (12.4), Dydimopanix morototoni (14.5), Ficus obtusifolia (13.8), Luehea seemannii (10.43) and Pseudobombax septenatum (13.1), during the wet season in a Central American semi-deciduous tropical forest in Panama, and the values measured by Hiremath (2000) in leaves of tropical fast-growing native trees of Costa Rica, Cedrela odorata (10.10) Cordia alliodora (12.12) and Hyeronima alchorneoides (8.07).

At the normal growth conditions, the values of the Ci/Ca ratio were nearly constant but variable depending on the terrestrial biome types, with a tendency to be relatively higher in tropical rainforest species than xerophytic or tropical dry forest tree species (Lloyd and Farquhar, 1994; Ehleringer and Cerling, 1995). The Ci/Ca ratio is also considered as a good indicator of the stomatal limitation of photosynthesis (Farquhar and Sharkey, 1982). In the case of plant species that are more conservative in relation to water use, the lower the values of the Ci/Ca ratio, the higher is the stomatal limitation of photosynthesis. As shown in Table 1, the maximum values of Ci/Ca ratios were observed at low values of D and high values of gs. For example, the maximum mean values of A and gs were observed for C. peltophoroides. At the same time, high values of the Ci/Ca ratio and low values of D were observed in this species.

Different equations were proposed in order to estimate the responses of stomatal conductance to the vapour pressure deficit, such as linear (Dolman and Van Den Burg, 1988; McCaughey and Iacobelli, 1993) or exponencial (Dye and Olbrich, 1993) functions. According to Landsberg and Hingston (1997), exponencial equations are advantageous to linear ones because the latter can estimate unrealistic negative values of stomatal conductance at high values of the vapour pressure deficit.

By contrast, the linear form permits the extrapolation of the values of D, when the estimated values of A or gs are near to zero. For stomatal conductance to water vapour, these values (estimated in our present study as g) were between 2 and 5 kPa in several tropical and temperate forest trees (Dolman and Van Den Burg, 1988; McCaughey and Iacobelli, 1993; Landsberg and Gower, 1997; Mielke et al., 1999). Because the stomata controls the exchange of CO₂ and H₂O between the leaf and the atmosphere, and the relationship of diffusion coefficients of CO₂ and H₂O is 1.6 (Nobel, 1991), we predicted that the estimated values of g for photosynthesis would be higher than the values estimated for the stomatal conductance to water vapour. Confirming these expectations, the estimated values of g for the Model 2 in our study varied between 4.64 for M. latifolium, and 6.31 kPa, for T. cacao (Table 2).

The best fittings obtained for Models 2 and 3 (Tables 2, 3 and 4) can be explained by the effects of D on stomatal conductance and net photosynthesis (Fig. 1). This occurred because a direct relationship between gs_sat and A_sat was observed for all studied species (Fig. 2) in a way similar to that which demonstrated for a countless number of tropical forest tree species (Hogan et. al., 1995; Ishida et al., 1996; Kitajima et al., 1997).

The values of A_max, a and Rd were related to the succesional status of an individual species, or group of species (Bazzaz and Picket, 1980; Lüttige, 1997). According to Lüttige (1997), the values of A_max in tropical plants were between 10 and 20 µmol CO₂ m^-2 s^-1 for sun plants, and between 1 and 3 µmol CO₂ m^-2 s^-1 for shade plants. We also need to consider that sunlight or shade tolerance varies if species are pioneer, late successional, understory or emergent canopy-dominant species. In this study, despite the fact that the trees of the different species analyzed were growing at different environmental conditions, it was clear that the highest value of A_max was observed in a fast-growing secondary species (C. peltophoroides) and the lowest value of A_max was observed in a typical late successional species (T. cacao). After correcting for the effects of D (based on the mean value of D for the all data collected, i.e. 1.70 kPa), the values of A_max estimated from the Model 3, for example, ranged from 7.00 up to 12.39 µmol CO₂ m^-2 s^-1 for T. cacao and C. peltophoroides, respectively.

In summary, the empirical mathematical models seemed to provide a good estimation of the light response photosynthetic parameters. When different photosynthetic characteristics of a particular species (or group of species) are to be compared, it is important to select an appropriate model and carefully indicate the environmental conditions at the moment in which the data are collected.

When the vapour pressure deficit inside the chamber is not controlled, the incorporation of linear or exponencial functions that explains the effects of the leaf-to-air vapour pressure deficit on leaf gas exchange is a very good method to enhance the performance of the models.

ACKNOWLEDGEMENTS

We thank Luiz Alberto Mattos da Silva for the taxonomic identification of the species and Brenda Colleen Clifton for English revision of the manuscript. We also thank José Inácio Lacerda Moura and Valdemicks dos Santos Muniz for the assistance in the research facilities and during the experimental evaluations. The financial support to the investigation was provided by Universidade Estadual de Santa Cruz (UESC).

Beyschlag, W. R. and Ryel, R. J. (1998), Modelling leaf/canopy photosynthesis. In: Raghavendra, A. S.(Ed.). Photosynthesis. A compreensive treatise. Cambridge: Cambridge University Press. pp. 305-319.

Farquhar, G. D. and von Caemmerer, S. (1982), Modelling of photosynthetic response to environmental conditions. In: Lange, O. L.; Nobel, P. S.; Osmond, C. B. and Ziegler, H. (Eds.). Encyclopedia of plant physiology. Berlin: Springer. v. 12B. pp. 549-587

Hogan, K. P.; Smith, A. P. and Samaniego, M. (1995) Gas exchange in six tropical semi-deciduous forest canopy tree species during wet and dry seasons. Biotropica, 27, 324-333.

Landsberg, J.J. (1986 ), Physiological ecology of forest production. Academic Press, San Diego

Landsberg, J. J. and Gower, S. T. (1997), Applications of physiological ecology to forest management. San Diego: Academic Press.

Leverenz, J. W. (1994), Factors determining the nature of the light dosage response curve of leaves. In: Baker, N. R. and Bowyer, J. R. (Eds.). Photoinhibition of photosynthesis. From molecular mechanisms to the field. Oxford: Bios Scientific Publishers. pp. 239-254.

Lüttge, U. (1997), Physiological ecology of tropical plants, Springer, Berlin

McMurtrie, R. E. (1993), Modelling of canopy carbon and water balance. In: Hall, D. O.; Scurlock, J. M. O.; Long, S. P. (Eds.). Photosynthesis and production in a changing environment: a field and laboratory manual. London: Chapman and Hall. pp. 220-231.

Nobel, P. S. (1991), Physiochemical and environmental plant physiology. San Diego: Academic Press.

Statsoft, Inc. (1995), Statistica for Windows. Tulsa.

Thornley, J. H. M. (1976), Mathematical models in plant physiology. A quantitative approach to problems in plant and crop physiology. London: Academic Press.

Received: February 16, 2004;

Revised: September 03, 2004;

Accepted: March 04, 2005.

• Aber, J. D.; Reich, P. B. and Goulden, M. L. (1996), Extrapolating leaf CO₂ exchange to the canopy: a generalized model of forest photosynthesis compared with measurements by eddy correlation. Oecologia, 106, 257-265.
• Barker, M. G.; Press, M. C. and Brown, N. D. (1997), Photosynthetic characteristics of dipterocarp seedlings in three tropical rain forest light environments: a basis for niche partitioning. Oecologia, 112, 453-463.
• Bazzaz, M. G. and Pickett, S. T. A. (1980), Physiological ecology of forest succession: a comparative review. Annual Review of Ecology and Systematics, 11, 287-310.
• Day, M. E. (2000), Influence of temperature and leaf-to-air vapor pressure deficit on net photosynthesis and stomatal conductance in red spruce (Picea rubens). Tree Physiology, 20, 57-63.
• Dolman, A. J. and Van Den Burg, G. J. (1988), Stomatal behavior in an oak canopy. Agricultural and Forest Meteorology, 43, 99-108.
• Dye, P. J. and Olbrich, B. W. (1993), Estimating transpiration from 6-year-old Eucalyptus grandis trees: development of a canopy conductance model and comparison with independent sap flux measurements. Plant, Cell and Environment, 16, 45-53.
• Ehleringer, J. R. and Cerling, T. E. (1995), Atmospheric CO₂ and the ratio of intercelullar to ambient CO₂ concentrations in plants. Tree Physiology, 15, 105-111.
• Eschenbach, C.; Glauner, R.; Kleine, M. and Kappen, L. (1998), Photosynthesis rates of selected tree species in lowland dipterocarp rainforest of Sabah, Malaysia. Trees, 12, 356-365.
• Evans, J. R.; Schortemeyer, M.; Farlane, N. and Atkin, O. K. (2000), Photosynthetic characteristics of 10 Acacia species grown under ambient and elevated atmospheric CO₂ Australian Journal of Plant Physiology, 27, 13-25.
• Farquhar, G. D.; von Caemmerer, S. and Berry, J. A. (1980), A biochemical model of the photosynthetic CO₂ assimilation in leaves of C₃ species. Planta, 149, 78-90.
• Franks, P. J. and Farquhar, G. D. (1999), A relationship between humidity response, growth form and photosynthetic operating point in C3 plants. Plant, cell and environment, 22, 1337-1349.
• Granier, A.; Huc, R. and Barigah, S. T. (1996), Transpiration of natural rain forest and its dependence on climatic factors. Agricultural and Forest Meteorology, 78, 19-29.
• Hiremath, A. J. (2000), Photosynthetic nutirent-use efficiency in three fast-growing tropical trees with differing leaf longevities. Tree Physiology, 20, 937-944.
• Ishida, A.; Toma, T.; Matsumoto, Y.; Yap, S. K. and Maruyama, Y. (1996), Diurnal changes in leaf gas exchange characteristics in the uppermost canopy of a rain forest tree, Dryobalanops aromatica Gaertn. f.. Tree Physiology, 16, 779-785.
• Kitajima, K.; Mulkey, S. S. and Wright, S. J. (1997), Seasonal leaf phenotypes in the canopy of a tropical dry forest: photosynthetic characteristics and associated traits. Oecologia, 109, 490-498.
• Kubiske, M. E. and Pregitzer, K. S. (1996), Effects of elevated CO₂ and light availability on the photosynthetic light response of trees of contrasting shade tolerance. Tree Physiology, 16, 351-358.
• Landsberg, J. J. and Hingston, F. J. (1996), Evaluating a simple radiation/dry matter conversion model using data from Eucalyptus globulus plantations in Western Australia. Tree Physiology, 16, 801-808.
• Lloyd, J. and Farquhar, G. D. (1994), ¹³C discrimination during CO₂ assimilation by the terrestrial biosphere. Oecologia, 99, 201-215.
• Loik, M. E. and Holl, K. D. (2001), Photosynthetic responses of tree seedlings in grass and under shrubs in early-successional tropical old fields, Costa Rica. Oecologia, 127, 40-50.
• Malhi, Y. and Grace, J. (2000), Tropical forests and atmospheric carbon dioxide. Tree, 15 : (8), 332-337.
• McCaughey, J. H. and Iacobelli, A. (1994), Modelling stomatal conductance in a northern deciduous forest, Chalk River, Ontario. Canadian Journal of Forest Research, 24, 904-910.
• Mielke, M. S.; Oliva, M. A.; Barros, N. F.; Penchel, R. M.; Martinez, C. A. and Almeida, A. C. (1999), Stomatal control of transpiration in the canopy of a clonal Eucalyptus grandis plantation. Trees, 13, 152-160.
• Nygren, P. (1995), Leaf CO₂ exchange of Erythrina poeppigoana (Leguminosae: Phaseolae) in humid tropical field conditions. Tree Physiology, 15, 71-83.
• Ögren, E. and Evans, J. R. (1993), Photosynthetic light response curves. I. The influence of CO₂ partial pressure and leaf inversion. Planta, 189, 182-190.
• Pachepsky, L. B. and Acock, B. (1996), An adequate model of photosynthesis _ II. Dependence of parameters on enviromental factors. Agricultural Systems, 50, 227-238.
• Prado, C. H. B. A.; Moraes, J. A. P. V. and Mattos, E. A. (1994), Gas exchange and leaf water status in potted plants of Copaifera langsdorffi I. Responses to water stress. Photosynthetica, 30, 207-213.
• Running, S. W. and Coughan, J. C. (1988), A general model of forest ecosystem processes for regional applications. I. Hydrologic balance, canopy gas exchange and primary production processes. Ecological Modelling, 42, 125-154.
• Sullivan, N. H.; Bolstad, P. V. and Vose, J. M. (1996), Estimates of net photosynthetic parameters for twelve tree species in mature forests of the southern Appalachians. Tree Physiology, 16, 397-406.
• Valladares, F.; Allen, M. T. and Pearcy, R. W. (1997), Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occuring along a light gradient. Oecologia, 111, 505-514.
• Yang, S.; Liu, X. and Tyree, M. T. (1998), A model of stomatal conductance in sugar maple (Acer saccharum Marsh). Journal of Theoretical Biology, 191, 197-211.

*

Author for correspondence

Publication Dates

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

History

• Accepted
  04 Mar 2005
• Reviewed
  03 Sept 2004
• Received
  16 Feb 2004