Oecologia (1997) 110:328–336 Springer-Verlag 1997 Mark E. Kubiske · Kurt S. Pregitzer · Carl J. Mikan Donald R. Zak · Jennifer L. Maziasz · James A. Teeri Populus tremuloides photosynthesis and crown architecture in response to elevated CO2 and soil N availability Received: 12 August 1996 / Accepted: 12 November 1996 Abstract We tested the hypothesis that elevated CO2 vesting for the lower crown. Only the mid-crown leaves would stimulate proportionally higher photosynthesis in at both N levels exhibited photosynthetic down regula- the lower crown of Populus trees due to less N retrans- tion to elevated CO2. Stem biomass segments (consisting location, compared to tree crowns in ambient CO2. Such of three nodes and internodes) were compared to the a response could increase belowground C allocation, total Aleaf for each segment. This analysis indicated that particularly in trees with an indeterminate growth pat- increased Aleaf at elevated CO2 did not result in a pro- tern such as Populus tremuloides. Rooted cuttings of portional increase in local stem segment mass, suggest- P. tremuloides were grown in ambient and twice ambient ing that C allocation to sinks other than the local stem (elevated) CO2 and in low and high soil N availability segment increased disproportionally. Since C allocated (89 ± 7 and 333 ± 16 ng N g–1 day–1 net mineralization, to roots in young Populus trees is primarily assimilated respectively) for 95 days using open-top chambers and by leaves in the lower crown, the results of this study open-bottom root boxes. Elevated CO2 resulted in sig- suggest a mechanism by which C allocation to roots in nificantly higher maximum leaf photosynthesis (Amax)at young trees may increase in elevated CO2. both soil N levels. Amax was higher at high N than at low N soil in elevated, but not ambient CO2. Photosynthetic Key words Carbon allocation · Elevated CO2 · N use efficiency was higher at elevated than ambient Nitrogen · Photosynthesis · Populus tremuloides CO2 in both soil types. Elevated CO2 resulted in pro- portionally higher whole leaf A in the lower three- quarters to one-half of the crown for both soil types. At Introduction elevated CO2 and high N availability, lower crown leaves had significantly lower ratios of carboxylation Photosynthetic carbon assimilation (A) is the primary V J transducer for energy flow from the abiotic to the biotic capacity to electron transport capacity ( cmax/ max) than at ambient CO2 and/or low N availability. From the top environment. A fundamental change in the efficient V J assimilation of C by plants would likely affect a number to the bottom of the tree crowns, cmax/ max increased in ambient CO2, but it decreased in elevated CO2 indicat- of plant, community, and ecosystem processes (Bazzaz ing a greater relative investment of N into light har- 1990; Field et al. 1992). In addition to being limited by soil N availability, C3 photosynthesis is presently limited M. E. Kubiske (&)1 · K. S. Pregitzer · J. L. Maziasz by atmospheric CO2 largely because O2 and CO2 com- School of Forestry and Wood Products, pete for the primary photosynthetic enzyme, ribulose- Michigan Technological University, 1,5-bisphosphate carboxylase/oxygenase (rubisco; Tol- Houghton, MI 49931, USA bert and Zelitch 1983). An increase in the ratio of C. J. Mikan · D. R. Zak atmospheric CO2:O2 favors carboxylation by rubisco, School of Natural Resources and Environment, enabling a greater amount of N invested in photosyn- The University of Michigan, Ann Arbor, MI 48109, USA thetic enzymes to be utilized in C fixation (Tolbert and Zelitch 1983; Sage 1994). A. Teeri Ample evidence exists for increased resource-use The University of Michigan Biological Station, The University of Michigan, efficiency and photosynthetic carbon assimilation by Ann Arbor, MI 48109, USA leaves and increased productivity in trees with an increase Present address: in atmospheric CO2 concentration (Poorter 1993; Ceule- 1Department of Forestry, Box 9681, mans and Mousseau 1994; Gunderson and Wullschleger Mississippi State, MS 39762-9681, USA 1994). In addition, studies indicate a change in C alloca- 329 tion patterns within individual trees in response to ele- Photosynthesis and crown architecture measurements vated CO2 that is highly dependent on soil N availability. Such a change in allocation could significantly affect Beginning in early September 1994, after 95 days of growth in the community and ecosystem processes, including species treatments, two ADC LCA-2 portable photosynthesis systems were used to measure instantaneous light-saturated photosynthesis per composition (Williams et al. 1986), belowground C stor- unit leaf area (Aarea) on every leaf attached to the main stem (n =4 age (Dixon et al. 1994), and ecosystem C and N cycling per CO2/fertility treatment) at 7- to 10-day intervals. There was not a substantial amount of self shading of the lower crown leaves in (Zak et al. 1993; Pregitzer et al. 1995). 2 At current CO concentrations, trees often exhibit a any treatment. On the same days that A was measured, a 1.7 cm 2 disk was punched from every third leaf on the main stem of the tree continual reallocation of N from lower, shaded leaves to for determination of N concentration (with a Carlo Erba NA1500 upper, sunlit leaves as the stem grows that is related to series II elemental analyzer), and specific leaf area (cm2 g–1). Leaf light availability and photosynthetic capacity (Field area was determined non-destructively by applying leaf length and 1983; Field and Mooney 1983; Sands 1995; Noormets width measurements to a predetermined regression equation: et al. 1996). In trees with an indeterminate growth pat- X ÿ X X area 3 38 0 20 length 018 width X tern, there is a mechanistic link between the location of 1 2 X assimilating leaves and the direction of C export from 0X01 length width r 099 those leaves (Dickson 1986, 1989). Most studies of tree A CIRAS-I portable photosynthesis system (PP Systems, response to elevated CO2 focus closely on factors Hitchin, UK) was used to construct A versus internal CO2 (Ci) affecting growth (C sinks) or on photosynthetic charac- relationships for leaves in the upper (first fully expanded leaf), mid, teristics of individual leaves (C sources), while we un- and lower portions of the crown. The CO2 concentration in air supplied to the leaf cuvette was increased from 100 to 1700 lmol derstand little about how the activity of C sources may mol–1 in seven increments under saturating irradiance (2250 lmol –2 –1 vary throughout the plant canopy in CO2 enrichment. m s ). This is particularly important because lower crown leaves are the sources for C allocation to belowground Photosynthesis analysis growth (Dickson 1986, 1989). Because elevated CO2 often results in higher photosynthetic N use efficiency, Photosynthesis per unit leaf area (Aarea) was calculated according we hypothesized that (1) lower crown leaves would re- to von Caemmerer and Farquhar (1981). The maximum A mea- tain a greater proportion of their original N, (2) there sured for each tree on each sample date was determined for com- parison with leaf N concentration. Whole leaf photosynthesis would be greater leaf mass in the lower crown due to (Aleaf) for every leaf was calculated from predicted leaf area and longer leaf retention, and (3) the distribution of whole- measured Aarea. We focused our analysis on Aleaf because it was a crown A would shift downward on the crown. better indication of total assimilation than Aarea. Whole leaf A,in To test these hypotheses, we measured leaf photo- turn, would be affected by leaf N content and leaf mass. Leaf mass of every third leaf was calculated from predicted leaf area divided synthesis, N, and mass throughout the crowns of Populus by specific leaf area. Whole leaf N content was calculated from N tremuloides trees grown at ambient and elevated CO2 and concentration and estimated leaf mass for every third leaf. In- in low and high soil N availability. To examine the effects stantaneous N-use efficiency (NUE) was calculated as lmol CO2 of a redistribution of A on C allocation, we measured the mol–1 Ns–1 for leaves in the upper, mid and lower portions of the architecture of the main stem and related those mea- crown. A/Ci relationships were analyzed by fitting the biochemical models of Farquhar and von Caemmerer (1982) and solving for surements to the distribution of A through the crown. V maximum carboxylation capacity ( cmax) and maximum rate of J electron transport ( max). Values of Vcmax, Jmax and NUE were analyzed as a split-plot ANOVA with crown position treated as a Methods sub-unit in the split-plot design. Means were compared with Fisher’s protected LSD procedure. Significance for all statistical Experimental design analyses was accepted at P 0.05. Rooted cuttings of wild clones of Populus tremuloides Michx. were Crown photosynthesis analyses planted in June 1994 in either low-N or high-N soil (89 ± 7 and 333 ± 16 ng N g–1 day–1 net mineralization, respectively) using Previous research has demonstrated that leaf initiation and devel- buried, open-bottom root boxes (0.5 m2 × 1.3 m deep) at the opment in young Populus trees occurs in proportion to the total University of Michigan Biological Station in northern lower number of leaves on the stem (Dickson and Shive 1982). Due to Michigan, United States. While four clones were planted into each large treatment differences in stem height and leaf numbers in this root box, a single clone was selected from each box for this study. study, leaves and stem segments were compared between treat- The high-N soil was the A-horizon of Kalkaska Sand (Typic ments by relativizing the vertical position on the stem, with 100 Haplorthod), and the low-N soil was a mixture of Kalkaska A- representing the apex.