Remobilization is an important mechanism of resource conservation in plants. However, our understanding of whether the responses of resource remobilization to global warming differ between deciduous and evergreen trees remains unclear. We assessed resource remobilization from leaves to 1-year-old shoots in a deciduous (
Plants reallocate resources from leaves to storage tissues prior to senescence, to support growth after dormancy (
The patterns of resource remobilization differ between deciduous and evergreen species (
Remobilization of plant’s N also differs between leaf habits of the species (
We investigated differences in resource remobilization between deciduous and evergreen species. Evergreen trees may maintain the resources directly in over-wintering leaves to reduce the costs of resource transport in the fall and next early spring, whereas deciduous trees need to reallocate resources from leaves to storage tissues in the fall to increase the resource use efficiency. In particular, we tested the hypotheses that: (1) both deciduous and evergreen trees reallocate resources from leaves to shoots at the end of growing season, but the former have higher resource remobilization than the latter; and (2) regardless of foliar habit, resource remobilization increases with increasing elevation (
The study was conducted in west Changbai Mountain, which is located in the Changbai Mountain Natural Reserve (41° 59′ N, 127° 59′ - 128° E) in Northeast China, and south Balang Mountain, which is located in the Wolong Natural Reserve (30° 53′ N, 102° 57′ E), at the eastern edge of Qinghai-Tibetan Plateau in Southwestern China.
At the Changbai Mountain site, the treeline elevation ranges from 2000 to 2030 m a.s.l., where groups of trees with height greater than 3 m have the deciduous broad-leaved
At the Balang Mountain site, pure evergreen broad-leaved
To compare the differences in concentrations of NSC and nutrients between leaves and shoots, and then to calculate the end-season remobilization rate between tissues, samples were taken at the end of growing season (September for Changbai Mt. in northeastern China and November for Balang Mt. in southwestern China), because end-season tissue NSC and nutrient concentrations are relatively stable (
To compare NSC and their composition (sugar:starch ratio) at different elevations, we measured the concentration of NSC using the anthrone colorimetric method, because few samples are required for microanalysis (
Oven-dried samples were ground to pass a 1 mm sieve. For each sample, 0.1 g of plant tissue was digested in 5 ml of H2SO4 and heated to boiling for 15 min. After cooling to room temperature, the digestion solution was added 2 ml H2O2 and then boiled for 15 min. The procedure described earlier was repeated until a colorless transparent liquid was produced. The total N concentration (% d.m.) was determined on a semi-automatic azotometer, and phosphorus was determined at 450 nm using a 721 spectrophotometer (
To clarify the remobilization of mobile carbohydrates and nutrients from leaves to shoots differences between deciduous and evergreen species at the end of growing season concentrations were expressed relatively to a constant parameter. Therefore, mobile carbohydrates, sugars, starch, N, and P remobilization efficiency (%) was calculated as (eqn. 1):
where
Given the large difference in elevation of the upper limit of the studied species, irrespective of the length of the growing season, the growing season soil (-10 cm) temperatures at their upper limit are the same being 6.5 ± 0.8 °C (
Elevation significantly affected tissue concentrations of soluble sugars, starch, NSC, N, and P, but it did not influence tissue sugars/starch (
Elevation significantly affected the remobilization efficiency of sugars, starch, NSC and N, but not P (
Tissue NSC concentration of
Both elevation and tissue type had significant effect on starch concentration (
Elevation had no effect on tissue N (
Trees at the highest elevation (2187 m a.s.l.) remobilized the highest quantities of sugars (
The concentration of leaf sugars had a relatively stable level across the elevational gradient, except for a higher level in trees at 3150 m a.s.l. and a lower level at 3450 m a.s.l. (
The N (
The remobilization of sugars, starch, and NSC from leaves to shoots showed similar elevational pattern (
Regardless of leaf habit, the concentration of NSC in leaves tended to decrease with increasing elevation (
Our results indicated that mobile carbohydrates for both deciduous and evergreen tree species were remobilized from leaves to shoots at the end of season, especially in the evergreen species (
We expected that the deciduous species had higher resource remobilization efficiency from leaves to shoots at the end of the growing season than the evergreen species. However, our results revealed a significantly lower mean remobilization efficiency of mobile carbohydrates from leaves to shoots in
The remobilization efficiency of sugars, starch and NSC was significantly higher in trees at their upper limit compared to lower elevations (
Deciduous trees showed a significantly higher mean sugars:starch ratio in tissues (4.33) than evergreen ones (1.70 -
There were no elevational effects on tissue N and P concentrations in both tree species (
Nutritional elements are crucial to growth, particularly N and P, which are the most important growth limiting nutrients (
N/P ratio has been applied to identify thresholds of nutrient limitation (
In line with our hypotheses, we found that mobile carbohydrates and nutrients (N and P), in both the deciduous and evergreen tree species, were remobilized from leaves to shoots at the end of season, and the remobilization efficiency was significantly higher in trees at the upper limit, helping trees to adapt to low temperature at high elevations. We also found that mobile carbohydrates, N and P had different patterns of leaf-to-shoot remobilization between the two species at the end of growing season. Compared to the deciduous
The present study contributes to better understand how trees adapt to growth-limiting temperatures at the alpine treeline, showing that the trees of mountain environments differ in their storage physiology, which may implicate heterogeneous distributional responses to climate warming. A limitation of the present study is that we were not able to quantitatively estimate the pool size of resource remobilization (concentration × biomass) from leaves to shoots (
This study was supported by the China Global Expert Recruitment Program (the Thousand Talents Plan), the National Key Research and Development Project (2016Y FA0602301), the National Natural Science Foundation of China (41371076; 41601052; 41501089), the China Postdoctoral Science Foundation (2015M580241), and the Fundamental Research Funds for the Central Universities (2412016KJ010). We thank Haibo Du, Kai Liu and Xiangyu Guo (School of Geographical Sciences, Northeast Normal University, Changchun, China) for their assistance in the field.
YC and AW contributed equally to this work.
Tissue mean concentration (mean ± SE; % of dry matter) of soluble sugars, starch, non-structural carbohydrates (NSC), sugars/starch ratio, and remobilization efficiency (R %) in
Tissue mean concentration (mean ± SE; % of dry matter) of total nitrogen (N) and phosphorus (P), N/P ratio, and remobilization efficiency (R %) in
Tissue mean concentration (mean ± SE; % of dry matter) of soluble sugars, starch, non-structural carbohydrates (NSC), sugars/starch ratio, and remobilization efficiency (R %) in
Tissue mean concentration (mean ± SE; % of dry matter) of total nitrogen (N) and phosphorus (P), N/P ratio, and remobilization efficiency (R %) in
Maximum and minimum daily mean air temperature (°C) at Changbai Mountain from late May to late September. Vertical grey line indicates the sampling date.
Characteristics of the plots and the sampling trees
Species and Site No. | Elevation(m) | Average | Slopeexposure | |
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DBH (cm) | Height (m) | |||
2187 | 1.1 ± 0.5a | 0.4 ± 0.1 | West | |
2137 | 1.6 ± 0.5a | 0.6 ± 0.1 | West | |
2097 | 1.5 ± 0.3a | 0.9 ± 0.1 | West | |
2027 | 4.9 ± 0.7 | 4.7 ± 0.3 | West | |
1977 | 28.4 ± 2.8 | 14.9 ± 0.9 | West | |
3589 | 5.5 ± 1.0 | 1.8 ± 0.6 | South | |
3441 | 7.4 ± 1.0 | 2.8 ± 0.5 | South | |
3327 | 5.1 ± 1.7 | 2.8 ± 0.9 | South | |
3159 | 5.6 ± 2.0 | 2.8 ± 0.9 | South | |
2978 | 7.1 ± 2.8 | 3.1 ± 0.7 | South | |
2843 | 8.2 ± 2.0 | 3.7 ± 0.3 | South |
Results of three-way nested ANOVAs with elevation, species, tissue type as factors. F and Prob values are given.
Factors | Soluble sugars | Starch | NSC | Nitrogen(N) | Phosphorus(P) | Sugars/Starch | N / P | |||||||
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Elevation (E) | 2.98 | 0.015 | 51.78 | <0.001 | 19.91 | <0.001 | 991.69 | <0.001 | 186.12 | <0.001 | 0.93 | 0.463 | 1.40 | 0.232 |
Species (S) | 494.79 | <0.001 | 64.23 | <0.001 | 205.03 | <0.001 | 258.08 | <0.001 | 10.30 | 0.002 | 652.27 | <0.001 | 19.20 | <0.001 |
Tissue type (T) | 444.99 | <0.001 | 1.81 | 0.182 | 286.78 | <0.001 | 3.11 | 0.012 | 0.34 | 0.886 | 331.66 | <0.001 | 2.07 | 0.154 |
E × S | 18.88 | <0.001 | 19.90 | <0.001 | 5.00 | 0.001 | 3.04 | 0.085 | 30.83 | <0.001 | 1.53 | 0.199 | 0.81 | 0.519 |
T × S | 804.41 | <0.001 | 5.71 | 0.019 | 517.92 | <0.001 | 3.28 | 0.009 | 0.52 | 0.763 | 315.12 | <0.001 | 16.45 | <0.001 |
E × T | 17.99 | <0.001 | 9.87 | <0.001 | 20.23 | <0.001 | 5.35 | 0.001 | 2.19 | 0.076 | 0.82 | 0.54 | 0.42 | 0.832 |
E × T × S | 4.07 | 0.004 | 4.34 | 0.003 | 5.09 | 0.001 | 2.58 | 0.042 | 0.89 | 0.475 | 0.91 | 0.46 | 0.53 | 0.716 |
Results of two-way nested ANOVAs with elevation and species as factors. The F and Prob values are given. R refers to remobilization efficiency.
Factors | R sugars | R starch | R NSC | R Nitrogen | R Phosphorus | |||||
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Elevations (E) | 18.69 | <0.001 | 9.20 | <0.001 | 50.98 | <0.001 | 4.78 | 0.001 | 0.74 | 0.600 |
Species (S) | 239.56 | <0.001 | 0.11 | 0.742 | 430.02 | <0.001 | 16.21 | <0.001 | 69.29 | <0.001 |
E × S | 20.31 | <0.001 | 8.16 | <0.001 | 46.16 | <0.001 | 2.93 | 0.030 | 0.81 | 0.528 |
Results of two-way nested ANOVAs with elevation and tissue type as factors. The F and Prob values are given.
Species | Factor | Solublesugars | Starch | NSC | Nitrogen(N) | Phosphorus(P) | Sugars/Starch | N / P | |||||||
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Elevations (E) | 11.93 | <0.001 | 3.47 | 0.018 | 12.74 | <0.001 | 3.71 | 0.013 | 2.28 | 0.080 | 0.60 | 0.670 | 4.38 | 0.006 |
Tissue types (T) | 925.90 | <0.001 | 23.95 | <0.001 | 557.60 | <0.001 | 59.85 | <0.001 | 6.19 | 0.018 | 184.12 | <0.001 | 53.52 | <0.001 | |
E × T | 4.54 | 0.005 | 0.11 | 0.979 | 3.43 | 0.019 | 2.31 | 0.078 | 0.32 | 0.861 | 0.51 | 0.731 | 1.92 | 0.129 | |
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Elevations (E) | 7.91 | <0.001 | 62.72 | <0.001 | 13.48 | <0.001 | 1.52 | 0.198 | 1.07 | 0.384 | 45.96 | <0.001 | 1.27 | 0.288 |
Tissue types (T) | 40.33 | <0.001 | 1.79 | 0.186 | 23.37 | <0.001 | 325.37 | <0.001 | 37.67 | <0.001 | 6.25 | 0.015 | 13.17 | 0.001 | |
E × T | 21.36 | <0.001 | 12.00 | <0.001 | 26.79 | <0.001 | 2.57 | 0.036 | 0.96 | 0.448 | 7.40 | <0.001 | 0.58 | 0.716 |