JOSÉ-LUIS MACHADO 1,3 and PETER B. REICH 2 1 Department of Biology, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081, USA - PDF

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Tree Physiology 26, Heron Publishing Victoria, Canada Dark respiration rate increases with plant size in saplings of three temperate tree species despite decreasing tissue nitrogen and nonstructural

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Tree Physiology 26, Heron Publishing Victoria, Canada Dark respiration rate increases with plant size in saplings of three temperate tree species despite decreasing tissue nitrogen and nonstructural carbohydrates JOSÉ-LUIS MACHADO 1,3 and PETER B. REICH 2 1 Department of Biology, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081, USA 2 Department of Forest Resources, University of Minnesota, 1530 Cleveland Ave. North, St. Paul, MN 55108, USA 3 Corresponding author Received August 6, 2003; accepted October 16, 2005; published online April 3, 2006 Summary In shaded environments, minimizing dark respiration during growth could be an important aspect of maintaining a positive whole-plant net carbon balance. Changes with plant size in both biomass distribution to different tissue types and mass-specific respiration rates (R d ) of those tissues would have an impact on whole-plant respiration. In this paper, we evaluated size-related variation in R d, biomass distribution, and nitrogen (N) and total nonstructural carbohydrate (TNC) concentrations of leaves, stems and roots of three cold-temperate tree species (Abies balsamea (L.) Mill, Acer rubrum L. and Pinus strobus L.) in a forest understory. We sampled individuals varying in age (6 to 24 years old) and in size (from 2 to 500 g dry mass), and growing across a range of irradiances (from 1 to 13% of full sun) in northern Minnesota, USA. Within each species, we found small changes in R d, N and TNC when comparing plants growing across this range of light availability. Consistent with our hypotheses, as plants grew larger, whole-plant N and TNC concentrations in all species declined as a result of a combination of changes in tissue N and shifts in biomass distribution patterns. However, contrary to our hypotheses, whole-plant and tissue R d increased with plant size in the three species. Keywords: Abies balsamea, Acer rubrum, balsam fir, biomass allocation, carbohydrates, deeply shaded, low light, Pinus strobus, red maple, root excavation, white pine, whole plant respiration. Introduction A positive balance between photosynthetic gains and respiratory losses allows plants to grow and reproduce. However, even under favorable growth conditions, on average, 40 to 60% of the photosynthates produced daily are lost in respiration (Kraus et al. 1989, Tjoelker et al. 1999a). In deeply shaded environments, dark respiration is likely to be a much greater fraction of total net carbon balance than in high-light conditions (Givnish 1988, Walters et al. 1993a). Therefore, a low mass-specific respiration rate (R d ) and associated low carbon losses are important components of both adaptation and acclimation to low-light environments (Reich et al. 2003). Reduced carbon losses (per unit mass invested) in low-light environments could occur as a result of decreased concentrations of substrates for respiration, e.g., total nonstructural carbohydrates (TNC), or lower R d for a given concentration of substrate. Tissue and whole-plant R d are likely dynamic with changing plant size. We predict that R d should decline with increasing plant size for three reasons. First, with increasing plant size, photosynthetic tissues likely decline as a fraction of wholeplant mass. Hence, declining R d with increasing size might be required to maintain stable whole-plant carbon balance. Second, as woody plants grow larger, the proportion of fine tissues (fine roots plus foliage), which have high R d, should decline in relation to coarser tissues (stems) with lower R d. The notion that R d should decline with plant size is consistent with data from laboratory studies showing that as young (first-year) plants or organs age and increase in size, their specific growth rates typically decrease and these changes are accompanied by decreases in R d (Poorter and Pothmann 1992, Walters et al. 1993b, Tjoelker et al. 1999a). Third, if trees enhance carbon conservation in deeply shaded environments, biomass should be distributed among plant tissues to lessen respiratory loads. Thus, as plants increase in biomass (size), there are likely concomitant changes in: (a) the proportion of respiratory versus photosynthetic tissues; (b) the proportion of tissues with different R d (e.g., stem versus leaves); and (c) the R d of any given tissue type. These respiratory and biomass distribution patterns are poorly characterized for perennial plants in the field. In this study, we evaluated the relationship between variation in plant size and tissue or whole-plant R d for three species that vary in observed shade tolerance and are common to the boreal and cold temperate forests of North America (Barnes and Wagner 1996): Abies balsamea (L.) Mill, Acer rubrum L. and Pinus strobus L., growing in moderately to deeply shaded understories (less than 13% of full sun) in northern Minnesota, USA. We measured R d, biomass distribution and concentrations of nitrogen (N) and TNC of leaves, stems and roots of 916 MACHADO AND REICH different sized saplings. We tested the following hypotheses: (H.1) R d declines with increasing shade (H.1A), and with increasing plant size (H.1B); (H.2) tissue N and TNC concentrations decline with increasing shade (H.2A) and with increasing plant size (H.2B); and (H.3) the fraction of whole-plant biomass distributed to foliage (the tissue type with the highest R d ) is negatively related to plant size but positively related to increased shading (Walters and Reich 1999). Materials and methods Study site The study area is located at the University of Minnesota s Cloquet Forestry Center in Cloquet, MN, USA (46 40 N, W). The stand was planted with white pine (Pinus strobus) in about 1930 after being cleared and burned of the original vegetation. The subcanopy and sapling layers are composed primarily of naturally regenerated red maple (Acer rubrum) and balsam fir (Abies balsamea) with lesser numbers of white pine, whereas the understory is mainly dominated by the shrub Corylus cornuta Marsh. Soils in the region are derived from glacial out-wash. The climate is cold-temperate continental with mean January and July temperatures of 12 and 20 C, respectively, and a growing season of about 120 days. Summer droughts are uncommon. Irradiance at systematic transects in the understory within the study area ranged from 1.0 to 41% of full sun during the summer (mean 11.2%) and 2.8 to 64.5% of full sun during the autumn (mean 26.5%, Machado 1999). Species and sapling selection In 1993, we determined the diameter at the stem base and total height of 1179 tree saplings in a systematic survey of 0.75 ha. In summer 1994, we measured percent canopy openness above each sapling with an LAI-2000 plant canopy analyzer (Li-Cor, Lincoln, NE). Percent canopy openness is a good surrogate of mean daily percent photosynthetic photon flux density for this forest cover (Machado and Reich 1999). Two canopy openness measurements at each plant were taken when the sky was uniformly overcast or 1 h after dawn and 1 h before dusk. We used one LAI-2000 at the measurement point (forest understory) while another paired unit simultaneously measured open sky values in a large clear-cut less than 1 km away. We averaged the two measurements for each plant. We sought to determine the effects of low-light environments and increases in plant size by selecting saplings (n =35 for each species) growing in the field across a range of plant heights (25 to 150 cm) and sapling light environments (1 to 13%). The selection of saplings was based on known plant light environments and heights of 1179 tree saplings allowing us to select both large and small saplings of each species growing in similar light environments, typically in close proximity, thus minimizing the possible effects of differences in microsite fertility or water availability, or both. To assess whether variation in mass was related to plant age, height or height growth rate and whether any or all of these varied systematically with light availability, we also assessed the relationships among these variables and their potential implications for interpreting the data. Sapling respiration measurements In 1995, from September 1 to September 18, nine individuals of each species were excavated. The remaining 26 individuals per species were excavated in 1996 between August 28 and September 15. These dates were selected to minimize the effect of active growth on R d. By the end of September almost all growth (excluding roots) ceases in conifer species that set bud (Kozlowski and Ward 1957a) and the broadleaf species start to drop their leaves (Kozlowski and Ward 1957b). All excavations were made between 0600 and 0900 h local time and we excavated 2 to 5 individuals per day depending on plant size. Immediately after excavation, the entire root system was covered with wet paper towels and the entire plant was covered with dark plastic bags. All plants were transported to a nearby laboratory at the field station where they were stored in a walk-in refrigerator at 5 C for no longer than 12 h from the time of excavation to the time of measuring respiration. Every day, plants were divided into leaves, stems and roots, and all the material was kept hydrated in the dark in a temperature-controlled growth chamber at 20 C for at least 2 h before any respiration measurements were made. All tissues were subsampled based on size and amount. Stems and roots were separated between coarse (more than 5-mm diameter) and moderately fine (less than 5-mm diameter). Rates of CO 2 flux were measured with open configuration, infrared gas analyzers and cuvettes (LCA-3 and PLC-C, Analytical Development, Hoddesdon, U.K.). Rates of net CO 2 efflux from intact roots free of soil and stems and leaves were measured separately in the dark at 20 C in a temperature-controlled growth chamber. Gas exchange measurements were taken after the readings had stabilized for at least 10 min. All plant material was dried in a forced air oven (70 C) and dry mass measured. Total nitrogen (N) concentrations of dried and ground tissues (mg N g 1 tissue) were measured by the Kjeldahl digestion assay (Research Analytical Laboratory, University of Minnesota). Total nonstructural carbohydrate (TNC) concentrations were determined as the sum of soluble sugar and starch assayed by the methods of Haissig and Dickson (1979) and Hansen and Møller (1975). Sugars were extracted from oven-dried and ground tissue in methanol:chloroform:water and tissue residuals were used for determination of starch content. For all plants, the following parameters were measured: height (cm), total foliage mass (g), total stem mass (g), total root mass (g) and age as number of rings at the base of stem (year). These data were used to determine the following biometric parameters: leaf mass fraction (LMF, g leaf g 1 total plant mass), stem mass fraction (SMF, g stem g 1 total plant mass), root mass fraction (RMF, g root g 1 total plant mass) and relative increase in height for 1993 and 1994 year ((Ln plant height in 1994 Ln plant height 1993) year 1 ). Finally, whole-plant R d (nmol CO 2 g 1 plant s 1 ) was calculated by summing root, stem and leaf R d weighted by the proportion of dry mass corresponding to each tissue. TREE PHYSIOLOGY VOLUME 26, 2006 RESOURCE CONSERVATION IN DEEPLY SHADED ENVIRONMENTS 917 Statistical analysis We conducted separate analyses for each species. First, variation in R d, N concentration and TNC concentration on tissue and whole-plant bases as a function of whole-plant mass, canopy openness and their two-way interaction were analyzed by multiple regression of natural log transformed response variables. These transformations were necessary to make the data approximately normal and to stabilize residual patterns. Second, we calculated the fraction of total plant R d and wholeplant mass for each of three tissues: leaves, stems and roots to test the extent to which whole-plant mass and canopy openness influence biomass distribution and respiratory costs. Variation for each tissue in the fraction of whole-plant R d and biomass distribution was analyzed as a function of wholeplant mass, canopy openness and their two-way interaction by multiple regression. Only whole-plant mass was natural log transformed. All analyses were conducted with JMP statistical analysis software (JMP 3.2, SAS Institute, Cary, NC). Results Relationships among plant height, growth, whole-plant mass and age Taller plants had more biomass than shorter plants (F ratio = 272, P for Abies; F ratio = 135, P for Acer; and F ratio = 205, P for Pinus). Plant height showed a significant increase in Pinus (F ratio = 8.8, P 0.006) and a significant decrease in Acer (F ratio = 8.7, P 0.007) in response to increases in light availability, although variation in irradiance explained only a small fraction of total variance (Figure 1). Light environments did not affect plant height in Abies. For each species, there were no significant whole-plant mass canopy openness interactions (data not shown). Given the strong correlation between height and mass, we do not distinguish between height and mass in the following discussion on plant size. In Pinus, the relative increase in height (a surrogate for plant relative growth rate), was negatively related to plant size (F ratio = 6.7, P = 0.005), whereas there was no relationship between relative height growth rate and size in the other species. In contrast, all species showed a significantly higher relative height growth rate with increasing canopy openness (F ratio = 10.7, P = for Abies; F ratio = 6.9, P = for Acer; and F ratio = 9.1, P = for Pinus). Despite their relatively small sizes, the saplings ranged in age between 7 and 24 years for Abies individuals (mean 14 years), 6 to 21 years for Acer individuals (mean 12 years) and 8 to 21 years for Pinus individuals (mean 14 years). However, larger plants were generally older (r 2 = 0.40, P = for Abies; r 2 = 0.49, P for Pinus; and not significant for Acer). Effects of plant size and low-light availability on R d Variations in irradiance had modest effects on R d in all species. Light was not significant as a main effect for whole-plant R d and was only significant for Acer stem R d (increase with light, F ratio = 14.2, P 0.001) and Pinus needle R d (decrease with light, F ratio = 6.8, P 0.013), generally refuting H.1A that plants of all species have lower R d with increasing shade. Furthermore, R d generally increased with plant mass (Figure 2), in direct contradiction to H.1B. Leaf, stem and whole-plant R d significantly increased with plant mass in all species, often doubling across the size range in each species (Figure 2). The R d of Abies roots was also greater in larger saplings (F ratio = 16.6, P 0.001). The relationships of R d with mass were independent of irradiance (no significant interactions). Figure 1. Changes in relative increase in height for 1993 and 1994 year (mm year 1, Panel a) and plant height (Ln mm, Panel b) as a function of percent canopy openness of naturally grown saplings in forest understories ranging in light from 1 to 13% canopy openness. The model included whole-plant mass (g), canopy openness (%) and two-way interaction. Only P values less than 0.05 are shown. Values represent measurements on single individuals. TREE PHYSIOLOGY ONLINE at 918 MACHADO AND REICH Figure 2. Changes in massspecific dark respiration rate (R d, nmol CO 2 g 1 s 1 ) for whole plant (Panel a), leaf (Panel b), stem (Panel c) and root (Panel d) as a function of whole-plant mass (g) of naturally grown saplings in forest understories ranging in light from 1 to 13% canopy openness. The model included whole-plant mass (g), canopy openness (%) and two-way interaction. Only P values less than 0.05 are shown. Values represent measurements on single individuals. Effects of plant size and low-light environment on N and TNC concentrations Increased shading generally did not lead to lower concentrations of whole-plant or tissue N or TNC concentrations, refuting H.2A. The exceptions included a decrease in whole-plant (F ratio = 8.2, P 0.001) and stem N concentrations with increasing shade in Pinus (F ratio = 9.7, P 0.004) and an increase in root TNC concentration with increasing shade in Acer (F ratio = 12.5, P 0.004). There were also several interactions of light with plant mass (data not shown). Whole-plant N concentration decreased with increasing plant mass in all species (Figure 3), supporting H.2B. This response was mainly driven by consistent decreases in stem and root N concentrations with increases in plant size (Figure 3). For TNC, there was some, but inconsistent, support for H.2B in all species (Figure 4). Among species, Acer had higher foliage N concentrations compared with the two conifers. However, whole-plant N concentration was not higher in Acer, because of the effects of species-specific differences in biomass distribution among leaves, stems and roots on wholeplant N concentration (Figure 3). We found large differences in tissue TNC concentrations among species. For example, foliage TNC concentration was 3 times higher in Abies than in Acer or Pinus, but TNC concentrations in stems and especially roots of Acer were 2 and 8 times higher, respectively, than those of the two conifer species (Figure 4). Distribution of biomass and whole-plant R d The distribution of biomass to different tissues varied with plant size in all species (Table 1 and Figure 5, Panel a). For Acer, leaf mass fraction (LMF) and root mass fraction (RMF) significantly decreased and stem mass fraction (SMF) in- TREE PHYSIOLOGY VOLUME 26, 2006 RESOURCE CONSERVATION IN DEEPLY SHADED ENVIRONMENTS 919 Figure 3. Changes in nitrogen concentration (mg N g 1 ) for whole plant (Panel a), leaf (Panel b), stem (Panel c) and root (Panel d) as a function of whole-plant mass (g) of naturally grown saplings in forest understories ranging in light from 1 to 13% canopy openness. The model included whole-plant mass (g), canopy openness (%) and two-way interaction. Only P values less than 0.05 are shown. Values represent measurements on single individuals. creased with increases in whole-plant size. Similar changes were found for RMF and SMF in Pinus and for RMF in Abies (Figure 5, Panel a; Table 1). Irradiance did not affect biomass distribution in Abies, whereas Acer and Pinus individuals had a greater fraction of biomass in roots and a lower fraction in stems (and also leaves for Acer), with increasing irradiance (data not shown; Table 1). Thus, with respect to H.3, the fractional distribution of biomass to foliage decreased with size and increased with light as hypothesized, but in only one of the three species studied. To evaluate the relative contributions to whole-plant R d of variations in biomass distribution and R d resulting from plant size and irradiance, we calculated the fraction of total plant R d in each of three tissues: leaves, stems and roots. Overall, the stem fraction of total plant R d was lower for Acer individuals compared with the conifer species (Figure 5, Panel b). For both Acer and Pinus species, the root and stem R d fractions of whole-plant R d decreased and increased, respectively, with plant size. This pattern largely resulted from size-related shifts in biomass distribution away from roots and leaves and towards stems (Figure 5, Panel a). For Acer, high R d of leaves resulted in a high foliar fraction of total R d at all plant sizes. Only for Pinus did we find significant responses of leaf and root fractions of whole-plant R d across light environments (data not shown). Discussion Acclimation of R d to low-light environment Overall, our data do not support the hypothesis that species reduce tissue or whole-plant carbon losses when growing in in- TREE PHYSIOLOGY ONLINE at 920 MACHADO AND REICH Figure 4. Changes in total nonstructural carbohydrate concentration (mg TNC g 1 ) for whole plant (Panel
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