Seasonal variation in the maximum rate of leaf gas exchange of canopy and understory tree species in an Amazonian semi-deciduous forest

RESEARCH ARTICLE

Seasonal variation in the maximum rate of leaf gas exchange of canopy and understory tree species in an Amazonian semi-deciduous forest

Kerrie M. Sendall^I, George L. VourlitisI,^*,Francisco A. Lobo^II

^IBiological Sciences Department, California State University, San Marcos, California, USA

^IIDepartamento de Solos e Engenharia Rural, Universidade Federal de Mato Grosso, Cuiaba', Mato Grosso, Brazil

ABSTRACT

Leaf gas exchange, water potential, and specific leaf area of two tropical semi-deciduous tree species, Brosimum lactescens S. Moore and Tovomita schomburgkii Planch & Triana, were quantified to establish how these properties were affected by seasonal variations in rainfall and leaf canopy position. The study was conducted at a site near Sinop Mato Grosso, Brazil, which is located within the ecotone of savanna and tropical rain forest. Both species exhibited significant declines in leaf water potential (Ψ_L), specific leaf area, area- and mass-based light saturated photosynthesis and dark respiration, and maximum stomatal conductance during the dry-season, suggesting that leaf structural properties and gas exchange are significantly altered by drought that develops during the 4-month dry season. Internal leaf CO₂ concentrations (C_i) were consistently lower during the dry season suggesting that the decline in maximum photosynthesis was due in part to a decline in stomatal conductance. However, seasonal variations in leaf gas exchange were larger for upper-canopy leaves, indicating an important interaction between drought stress and canopy position. The seasonal variation in leaf gas exchange and morphology was presumably due to a combination of drought stress and leaf lifespan. The results of this study suggest that drought has important implications for the leaf physiology and morphology of semi-deciduous Amazonian forest trees.

Key words: Brazil, Brosimum lactescens, climate change, ecotone, photosynthetic response, Tovomita schomburgkii, tropical transitional forest.

Introduction

Amazonian semi-deciduous forests are located within the savanna (cerrado)-rainforest ecotone along the southern and eastern borders of the Amazon Basin. Under current climate conditions the annual carbon budget of these forests appears to be in balance (Vourlitis et al. 2001, 2004, 2005; Keller et al. 2004: Priante et al. 2004). However, semi-deciduous forests of the southern Amazon Basin have experienced significant temperature increases over the last 30 years (Malhi and Wright 2005) and are also subjected to periodic warming and drought during El Niño (Potter et al. 2004). Drought can reduce net primary production (NPP), net ecosystem production (NEP), and evapotranspiration (Nepstad et al. 2002; Priante et al. 2004; Vourlitis et al. 2002, 2008), and cause an increase tree mortality (Condit et al., 1995). Thus, understanding how drought influences rates of C and H₂O exchange is important for understanding current and future rates of NPP, NEP, and evapotranspiration.

Seasonal patterns of C and H₂O exchange are affected by variations in leaf gas exchange, which in turn are regulated by a trade-off between seasonal patterns in rainfall and light availability. While these variations may be small in amplitude, they can significantly alter the physiological behavior of plants (Hogan et al. 1995; Miranda et al. 2005). In general, rates of photosynthesis increase considerably during the wet-season, even though an increase in cloudiness can limit light availability, because plants are exposed to high levels of soil water content, while declines in water availability during the dry season cause an overall reduction in leaf water potential and maximum photosynthesis (Pearcy 1987, Miranda et al. 1996, Sun et al. 1996, Miranda et al. 2005). However, the effects of seasonal drought are not likely to be similar for canopy and understory leaves and trees because of differences in physiology and resource allocation, phenology, and/or canopy growth microclimate (Boardman 1977; Cabral et al. 1996). For example, canopy trees are exposed to higher light, warmer temperatures, and lower atmospheric humidity than understory trees (Cabral et al. 1996), which can limit rates of gas exchange (Chaves et al. 1992). Leaves in the upper-canopy may have higher tissue N concentration, which will afford higher rates of maximum photosynthesis but at a higher respiratory cost (Reich and Walters 1994; Meir et al. 2001). Large trees may also have deep roots with access to water that can sustain high rates of gas exchange during the dry season (Nepstad et al. 1994).

Although a good deal of research has addressed how drought and light availability affect rates of photosynthesis in tropical forests, less is known about how these rates are affected by seasonality. This research is especially important in seasonally dry tropical forests, which experience significant temporal variation in rainfall and soil water content. Climate change from deforestation and fossil fuel combustion is anticipated to increase the magnitude and/or duration of seasonal drought (Cramer et al. 2005; Cowling et al., 2005), and semi-deciduous tropical forests are likely to be very sensitive climate change due to their transitional nature (Longman and Jenik 1992; Arris and Eagleson 1994). Thus, the objective of this study was to evaluate how leaf gas exchange and related traits were influenced by seasonality and canopy position in a semi-deciduous, tropical transitional forest in the southern Amazon Basin. We hypothesize that seasonal variations in gas exchange will be large and correlated with variations in rainfall; however, the magnitude of the seasonal variation in gas exchange will be a function of canopy position.

Materials and methods

Site and species descriptions: The study was conducted in an intact, mature, upland (terra firme) semi-deciduous forest located near Sinop, Mato Grosso, Brazil (11°24.75'S; 55°19.50'W) at an elevation of 423 m above sea level. This region is within the rainforest-savanna transition zone, which in northern Mato Grosso lies between 9 and 14°S latitude (Ackerly et al. 1989). Maximum canopy height is 25-28 m, and a survey of the area indicated that there are 35 families and 80 species of trees with a diameter ≥ 10 cm, including Protium sagotianum Marchland, Brosimum lactescens (S. Moore) C. C. Berg, Tovomita schomburgkii Planch & Triana, and Qualea paraensis Ducke. However, three species, P. sagotianum (Burseraceae), B. lactescens (Moraceae), and T. schomburgkii (Clusiaceae), make up about 50% of individuals. Leaf area index (LAI) varies between 6.0 m²m^-2 at the end of the wet season (April) and 2.5 m²m^-2 at the end of the dry season (August) reflecting the semi-deciduous nature of the forest (Vourlitis et al. 2004; Sanches et al. 2008a). The soil is a quartzipsamments with a sandy, porous texture that drains rapidly after rainfall. The mean annual air temperature is approximately 24°C, and average annual rainfall is about 2.0 m (Vourlitis et al. 2002). About half of the annual rainfall is received during the December-February wet season while only about 1% occurs during the June-September dry season (Vourlitis et al. 2002).

Two species located near a 40 m tall tower at the study site were selected for measurement due to their proximity to the tower or because they were short enough to be measured from the forest floor. Brosimum lactescens (Moraceae) is a semi-deciduous canopy emergent tree found in Amazonian evergreen and semi-deciduous forests (Ackerly et al. 1989, Lorenzi 2000). At our study site this species is 25-28 m tall with an average (± 1 SD) diameter of 24.6 ± 11.5 cm. Tovomita schomburgkii (Clusiaceae) individuals are 4-17 m tall and are found in Amazonian forests in northeastern and central Brazil (Mariz 1974). At our study site these species account for 30% of all trees ≥ 10 cm diameter.

Gas exchange measurements: Photosynthetic light-response curves were generated using a portable photosynthesis system (model LI-6400, LI-COR, Lincoln, NE., USA). One B. lactescens and three T. schomburgkii individuals were sampled during each season, because these trees were accessible either from the forest floor or from the tower at varying heights. In order to obtain multiple in situ measurements high within the forest canopy the leaves had to be readily accessible from the tower, which is why only one B. lactescens individual was sampled.

B. lactescens leaves were measured at canopy heights of 28, 20, and 12 m, while T. schomburgkii leaves were measured at 12, 10, and 1 m. Twelve light curves were generated at each of these heights during both the dry (July 2005) and wet (January 2006) seasons. To determine the effect of humidity on leaf gas exchange half of the light curves (n = 6) were generated at a relative humidity of 40% and half were generated at a relative humidity of 70%. These humidity levels corresponded to a leaf-air vapor pressure deficit of 2.6 kPa and 1.5 kPa, respectively given the temperature conditions associated with the photosynthesis measurements, and are indicative of the mid-day relative humidity and atmospheric vapor pressure deficit that canopy leaves are exposed to during the dry and wet seasons, respectively (Vourlitis et al. 2004; 2005, 2008). Leaves were exposed to 400 mmol mol^-1 CO₂ and photosynthetic photon flux density (Q) levels of 2000, 1500, 1000, 500, 250, 100, 50 and 0 mmol quanta m^-2s^-1 using the LI-6400 LED light source. Chamber temperature was held at 28°C for all measurements.

Additional measurements: Leaf water potential (Ψ_L) was measured after every light curve using a pressure chamber (model 670, PMS Instrument Company, Albany, OR, USA) on fresh leaves adjacent to those measured for gas exchange. After measurement of Ψ_L digital photos were taken of the leaves and the one-sided area was quantified using digital-image processing software (Sigma Scan Pro, version 5.0, Aspire Software International, Leesburg, VA, USA). Leaves were then dried at 70 °C for at least 48 hours to determine dry mass, and the projected specific leaf area (SLA) was calculated as the ratio of one-sided leaf area per unit dry weight.

Data analysis and photosynthesis modeling: Area-based photosynthetic data were fitted to a model that estimated net CO₂ assimilation (P_net; mmol CO₂ m^-2s^-1) as a function of Q:

where Φ = the maximum quantum yield (mmol CO₂ mmol Q^-1), P_marea = the maximum area-based rate of net photosynthesis (mmol CO₂ m^-2s^-1), and θ = the dimensionless convexity of the curve (Thornley 1976, Ögren and Evans 1993). Non-linear least squares regression was used to estimate the model coefficients (θ, Φ and P_marea). Maximum stomatal conductance (g_max), and internal CO₂ concentrations (C_i) were calculated using the portable photosynthesis system using the same levels of CO₂, irradiance, temperature, and relative humidity discussed above, while area-based dark respiration (R_darea) was calculated when Q = 0 mmol quanta m^-2s^-1. Mass-based maximum photosynthesis (P_mmass) and dark respiration (R_dmass) rates were calculated by multiplying area-based rates by SLA.

Variations in Ψ_L and SLA across season and canopy height were statistically evaluated using a two-factor analysis of variance. Multivariate analysis of variance (MANOVA) was used to determine whether there were differences in P_marea, P_mmass, R_darea, R_dmass, g_max, and C_i across season, height, and relative humidity. The response of these variables as a function of season and canopy height did not differ with humidity, so in further analyses data were pooled across humidity. In the event of a significant season x height interaction a one-way analysis of variance was used to determine whether differences existed across height and/or season.

Results

Leaf water potential and specific leaf area: Leaf water potential (ψ_L) declined during the dry season for T. schomburgkii and B. lactescens, but understory leaves experienced a smaller seasonal decline in ψ_L than mid- and upper-canopy leaves (Figure 1). For example, the ψ_L of T. schomburgkii mid-canopy leaves (12 m) was approximately 0.3 MPa lower during the dry season, while the average decline in ψ_L for T. schomburgkii understory leaves (10 m and 1 m) was only about 0.15 MPa. The ψ_L of B. lactescens upper-canopy (28 m) and mid-canopy ( 20 m and 12 m) leaves was on average 0.65 MPa lower during the dry season.

The specific leaf area (SLA) of T. schomburgkii differed significantly among seasons and canopy heights; however, B. lactescens leaves only exhibited statistically significant differences in SLA on a seasonal basis (Figure 2). During the dry season, the SLA for T. schomburgkii ranged from an average (± SD) of 198 ± 50.1 cm² g^-1 in the forest understory to 73 ± 25.8 cm² g^-1 in the mid-canopy, while during the wet season, the average SLA of mid-canopy leaves increased by almost 30%. Seasonal variation in SLA notwithstanding, the SLA of T. schomburgkii was negatively correlated with height. In contrast, seasonal variations in SLA were significantly positively correlated with leaf water potential for B. lactescens. The SLA of both mid-canopy and upper-canopy leaves of B. lactescens was approximately 83 cm² g^-1 during the dry season, but during the wet-season, the SLA of upper-canopy leaves remained at 85 cm² g^-1 while mid-canopy leaves showed an increase of more than 20% to 110 ± 6.3 cm² g^-1 (Figure 2).

Leaf gas exchange: The photosynthetic light-response of both tree species was well described by equation 1, and the coefficient of determination (r²) values ranging between 0.95-0.97 (Table 1). The effect of humidity on the estimated coefficients was minimal; however, both species exhibited consistent seasonal differences in the quantum yield (Φ), maximum rate of light-saturated photosynthesis (P_marea), and the convexity index of the hyperbolic curve (Table 1). Values of the Φ and P_marea were on average 2 and 1.7-times higher during the wet-season, while values of the convexity index were about 50% lower in the wet-season indicating a lower propensity of leaf photosynthesis to saturate at higher levels of Q.

The results of the MANOVA indicated a significant main effect of season and height, and a significant season by height interaction on area- and mass-based light saturated photosynthesis (P_marea, P_mmass), area- and mass-based dark respiration (R_darea, R_dmass), maximum stomatal conductance (g_max), and internal CO₂ concentration (C_i) (Table 2). Both species, regardless of their canopy position, exhibited significantly higher rates of P_marea during the wet season, though the smallest increases were seen in understory leaves (Figure 3). Upper-canopy (20 and 28 m) B. lactescens and mid-canopy (12 m) T. schomburgkii leaves exhibited the highest rates of P_marea, with mean (± SD) rates of 7.2 ± 0.84 and 7.9 ± 0.81 mmol CO₂ m^-2s^-1, respectively. Mid-canopy T. schomburgkii leaves experienced a 40-50% increase in P_marea during the wet season, while understory leaves exhibited smaller increases of 15-30%. Upper-canopy leaves of B. lactescens experienced a 40-55% increase in P_marea, while mid-canopy leaves increased by 25-30%. P_marea increased with canopy height during both the wet and dry seasons in T. schomburgkii leaves, but increases with height were only observed during the wet season for B. lactescens. Rates of P_mmass responded similarly to rates of P_marea (data not shown), increasing significantly during the wet season at all canopy heights; however, canopy position did not have as large an effect on rates of P_mmass.

Average rates of R_darea and R_dmass were also consistently higher during the wet season for both species. The smallest seasonal variation in R_darea was observed in the understory and upper-canopy leaves, which experienced increases of 15-25% in the wet season, whereas mid-canopy leaves displayed seasonal increases of 30-50% (Figure .4). R_darea also tended to increase with height in the forest canopy where leaves were exposed to more sunlight. The R_dmass (data not shown) response to canopy height in both species was very similar to the response of P_mmass, with B. lactescens exhibiting very little change with canopy height within season and T. schomburgkii exhibiting large differences in the dry season only.

During the dry season, maximum stomatal conductance (g_max) was consistently less than 65 mmol m^-2s^-1 at all canopy heights; however during the wet season, g_max increased considerably in leaves higher in the canopy that are exposed to higher levels of irradiance, reaching levels as high as 175 mmol m^-2s^-1 (Figure 5). Understory leaves also experienced an increase in g_max during the wet-season, but it was much smaller than in leaves exposed to more sunlight. Mid-canopy (12 m) B. lactescens leaves exhibited an increase of 52-57% while the understory leaves of T. schomburgkii had the smallest increase of 18-42%.

Values of C_i were consistently higher in the wet-season than in the dry season (Figure 5). The largest seasonal differences in C_i were observed in mid- and upper-canopy plants, which exhibited increases of 7-12% in the wet season, while smaller increases were observed in the understory, ranging from 0-5%. The average (± SD) ratio of internal CO₂ concentration (C_i) to ambient atmospheric CO₂ (C_a) was 0.64 ± 0.03 during the dry season and 0.71 ± 0.03 during the wet season. The optimal ratio for C₃ plants is 0.70 (Wong et al. 1979), which indicates that photosynthesis may have been limited by available internal CO₂ during the dry season (Miranda et al. 2005).

Discussion

We hypothesized that the leaf gas exchange of T. schomburgkii and B. lactescens would be significantly lower in response to seasonal drought; however, the decline in gas exchange would be larger for leaves in the upper canopy. Our results support this hypothesis, as all measures of leaf gas exchange were significantly lower during the dry season and the significant season x height interaction indicates that the sensitivity of seasonal drought was dependent on canopy position (Table 2).

Large seasonal variations in leaf gas exchange were expected given that the majority of the rainfall in this region falls during the wet season, while only 1% falls during the dry season (Vourlitis et al. 2002, Keller et al. 2004). Since the soils in the study site drain rapidly after rainfall, the forest can experience significant drought during the dry season (Malhi et al. 1998, Williams et al. 1998). With drought plants tend to close their stomata due to increasing evaporative demand at the surface of the leaf, which in turn decreases leaf photosynthetic rates (Meinzer et al. 1993), and even slight decreases in leaf water potential (Ψ_L) can trigger stomatal closing (Wright et al. 1992, Allen and Pearcy 2000). Interestingly, recent data suggests that rates of sap flow for B. lactescens and T. schomburgkii and whole-forest evapotranspiration may be relatively stable over seasonal cycles (Vourlitis et al. 2008), suggesting that plants have access a stable groundwater source (Nepstad et al. 1994). The stability in canopy evapotranspiration appears to be driven by seasonal trade-offs in net radiation (lower in the wet season due to cloud cover) and atmospheric evaporative demand (higher in the dry season due to lower atmospheric humidity). The high evaporative demand experienced during the dry season, coupled with possible limitations in hydraulic conductance, would lead to a decline in Ψ_L and g_max (Meinzer et al. 1993; Vourlitis et al. 2008).

Understory leaves of T. schomburgkii experienced the smallest seasonal variation in P_marea, P_mmass, and g_max, perhaps because these leaves are exposed to lower levels of sunlight and experience a lower evaporative demand (Whitehead et al. 1981, Tobin et al. 1999). These tree species also exhibited smaller seasonal variations in sap flow than taller trees in the forest canopy (Vourlitis et al. 2008), suggesting more consistent seasonal rates of leaf gas exchange. The internal CO₂ concentrations (C_i) of these understory leaves remained relatively constant between seasons, decreasing by less that 6% during the dry season, indicating relatively small stomatal limitations to CO₂ diffusion. Upper-canopy B. lactescens leaves and mid-canopy leaves of both species exhibited substantially larger seasonal variation in P_marea, P_mmass, and g_max than understory T. schomburgkii leaves. In all cases, the Ψ_L in the mid- and upper-canopy was significantly higher during the wet season, so it appears that these leaves experienced less water stress during the wet season and were able to increase levels of stomatal conductance (Whitehead et al. 1981; Yordanov et al. 2000). However, the significant increase in photosynthetic rates that was observed in upper-canopy leaves does not appear to be fully explained by the increased diffusion of CO₂ considering that the C_i during the wet season increased by only as much as 12%. Additionally, the increase in photosynthetic rates during the wet season did not coincide with increased leaf nitrogen (data not shown), which is known to affect the rate at which plants can fix CO₂ for use in photosynthesis (Evans 1989).

Large seasonal variation in P_marea, P_mmass, and g_max may have been caused in part by differences in leaf age (Hogan 1988; Reich et al. 1991; Osada et al. 2001). Leaves generally develop and become fully expanded during the wet season when photosynthetic rates, SLA, and stomatal conductance are highest (Miyaji et al. 1997). These leaf traits are negatively correlated with leaf age (Chabot and Hicks 1982; Field and Mooney 1986) and decline throughout the year until the dry season when leaf shedding occurs in response to drought (Reich and Borchert 1984; Sanches et al. 2008b).

Our data suggest that seasonal variations in rainfall distribution and drought significantly alter the leaf gas exchange of tropical understory and canopy tree species. These data are consistent with other studies in tropical savanna (Franco 1998; Prado et al. 2004), semi-deciduous forest (Hogan et al. 1995; Miranda et al. 2005), and rainforest (de A. Sa et al. 1996; Bonal et al. 2000), and suggest that periodic drought represents a key control on tropical tree productivity. Given the anticipated 3-4ºC increase in average annual temperature for the Brazilian tropics (Giorgi et al. 2001), the potential magnitude and/or duration of seasonal drought is likely to increase. Anticipated changes in precipitation are expected to be small, ranging from 0.0-1.0 mm d^-1, but many models predict an intensification of the dry season in eastern South America (Malhi et al. 1999; Giorgi et al. 2001). Higher temperatures may lead to increased water stress (Malhi et al. 1999), and species that are more vulnerable to decreases in water potential will have a decreased gas exchange and likelihood of survival. Thus, changes in gas exchange may significantly alter the species composition and productivity.

Acknowledgments: This research was supported by the National Science Foundation, Division of Environmental Biology-Ecosystem Studies (DEB-0343964). Additional support was provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), California State University, San Marcos (CSUSM), and the Universidade Federal de Mato Grosso (UFMT). The authors thank O. Borges and P. Bambi for field and laboratory assistance.

RUNNINH HEAD: Gas exchange of tropical semi-deciduous forest trees.

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Publication Dates

• Publication in this collection
  17 Dec 2009
• Date of issue
  2009

History

• Accepted
  04 June 2009
• Received
  31 Mar 2009