Restoring temperate secondary forests by promoting sprout regeneration: Effects of gap size and within-gap position on the photosynthesis and growth of stump sprouts with contrasting shade tolerance

Forest Ecology and Management 429 (2018) 267–277

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Restoring temperate secondary forests by promoting sprout regeneration: Effects of gap size and within-gap position on the photosynthesis and growth of stump sprouts with contrasting shade tolerance

T

⁎

Ting Zhanga,b,c, Qiaoling Yana,b, , Jing Wanga,b,c, Jiaojun Zhua,b a

CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Shenyang 110016, China Qingyuan Forest CERN, Chinese Academy of Sciences, Shenyang 110016, China c University of Chinese Academy of Sciences, Beijing 100049, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Foliage traits Growth Photosynthetic response Stump sprouts Restoration of secondary forests

To improve the productivity and ecological functions, it is essential to recover secondary forests, the major forest resources in the world, by promoting the regeneration of dominant tree species. Forest gaps are a dominant form of small-scale disturbances in secondary forests, and sprout regeneration commonly occur after the gap formation from logging. Within-gap position and gap size are two key characteristics affecting tree regeneration by changing micro-environments. Promoting the sprout regeneration of dominant tree species under forest gaps with various sizes and within-gap positions is a key measure to recover secondary forests. Twelve artificial gaps were created in March 2015 and the photosynthesis and growth of stump sprouts of three dominant tree species with varying levels of shade tolerance (Quercus mongolica, Acer mono, and Tilia mandshurica) were monitored in 2016. The results showed that within-gap position and gap size had significant effects on the photosynthetic ability of stump sprouts of Q. mongolica, i.e., the moderate light condition at the center parts of large gaps was more beneficial to its photosynthesis with the maximum PNmax of 26.49 μmol m-2 s-1. Gap size significantly affected the biomass of stump sprouts of both Q. mongolica (shade intolerant tree species) and A. mono (intermediate shade tolerant tree species), e.g., the aboveground biomass of these two tree species in large gaps (178.90 g for Q. mongolica and 158.42 g for A. mono, respectively) were significantly higher than those in small gaps (50.52 g for Q. mongolica and 56.95 g for A. mono, respectively) (P < 0.05). It can be concluded that of the three tree species in this study, only Q. mongolica and A. mono are sensitive to the changing environments caused by the gap size and within-gap position at the early stage of gap formation, and their photosynthesis and growth can be promoted in large gaps and at the central part of gaps with moderate light conditions. Consequently, when logging trees to create gaps, forest managers can control the gap size and within-gap position where target trees are located to promote their stump sprouts regeneration. This study may provide a new insight for the directed cultivation and restoration of temperate secondary forests.

1. Introduction Secondary forests, derived from the natural regeneration of primary forests after destructive disturbances (e.g., extreme natural disasters and human activities) (Yan et al., 2010), have become major forest resources in China, accounting for more than 50% of the total area of national forests (Zhu et al., 2007a). Compared with primary forests, several problems have been observed in broadleaved secondary forests, including unoptimizable stand structure, unsuccessful natural regeneration of dominant tree species and unsustainability in both ecosystem services and productivity (Zhu and Liu, 2004; Zhu and Liu,

⁎

2007). Moreover, secondary forests are going through a variety of disturbances; forest gaps created by the death or fall of one or more trees (Runkle, 1982) are recognized as a dominant form of small-scale disturbances playing a critical role in forest regeneration and succession in secondary forests (Zhu and Liu, 2004; Kneeshaw and Prévost, 2007; Gendreau-Berthiaume and Kneeshaw,2009; Yan et al., 2010). One principal goal of forestry development is to facilitate the regeneration of dominant tree species to recover secondary forests (Gu et al., 2005; Yan et al., 2010). Therefore, promoting natural regeneration under forest gaps is one of the key measures to achieve this development goal (van Kuijk et al., 2008).

Corresponding author at: Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China. E-mail address: [email protected] (Q. Yan).

https://doi.org/10.1016/j.foreco.2018.07.025 Received 14 March 2018; Received in revised form 24 June 2018; Accepted 9 July 2018 0378-1127/ © 2018 Elsevier B.V. All rights reserved.

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damage by high irradiance (He et al., 2010). To promote sprout regeneration in gaps, it is vital to discover how the photosynthesis and growth of stump sprouts respond to variations in the micro-environment caused by gap size and within-gap position. The main objectives of this study were to: (1) quantify the responses of the sprout regeneration performance (including photosynthesis, foliage traits and growth fitness) of three broadleaved tree species with varying levels of shade tolerance to the changes in the micro-environment caused by varying gap sizes and within-gap positions and (2) determine the optimum size and within-gap position for promoting stump sprout regeneration of these three broadleaved species. This study may provide some scientific references for the restoration of temperate secondary forests by promoting sprout regeneration in forest gaps.

After gap formation in broadleaved secondary forests, there are two sources of natural regeneration: seed regeneration and sprout regeneration. Seed regeneration can be used to predict the direction of future regeneration (Bellingham, 2000); the regenerated stump sprouts after gap formation can grow much faster than seedlings germinated from seeds to quickly occupy the gap environment (Bond and Midgley, 2001). Previous studies have been concerned on the effects of gaps on seed regeneration (e.g., seed rain, soil seed bank, and seedling emergence from seeds) in forest ecosystems (e.g., Albanesi et al., 2008; Yan et al., 2010, 2012). However, restoration of gaps at the early formation stage in temperate secondary forests may mostly rely on vegetative propagation of species (e.g., sprout regeneration) rather than seed regeneration (Yan et al., 2010). Unfortunately, compared with the achievements on seed regeneration, less is known about the characteristics of sprout regeneration in forest gaps in secondary forests (Feng et al., 2011). There are some researches on sprout regeneration of woody plants (Tredici, 2001; Mostacedo et al., 2009; Mc Carthy et al., 2014), and most of them have mainly concentrated on sprouting mechanisms (e.g., there are six hypotheses for the sprouting mechanisms of woody plants) (Zhu et al., 2007c), effects of stump traits (e.g., basal diameter and height) on sprout survival and growth (Huang, 1990; Wang et al., 2004), and sprout regeneration after a fire (Vesk and Westoby, 2004). Sprouting in many woody angiosperms is common (Wells, 1969), and the success of sprout regeneration for many woody angiosperms species is important to their regeneration. This is mainly because seedling survival and establishment phases are the key bottlenecks in the seed regeneration processes and strongly rely on both abiotic factors (e.g., the light environment) and inherent biotic factors (e.g., shade tolerance of the tree species and nutrient storage from falling trees/stumps) (Poorter and Kitajima, 2007; Bace et al., 2011). However, sprout regeneration is less restricted by site conditions (Su et al., 2012) due to the fact that sprouts can obtain enough nutrients and micronutrients from stumps or roots to maintain growth (Iwasa and Kubo, 1997; Zhu et al., 2007c). As two key characteristics of forest gaps, gap size and within-gap position play a crucial role in the natural regeneration of tree species by affecting the gap micro-environment (e.g., Gray and Spies, 1996; Ritter et al., 2005; Albanesi et al., 2008; He et al., 2012; Čater et al., 2014). Variations in gap sizes and within-gap locations first lead to changes in light conditions in forest stands and further affect the spatial and temporal distribution features of other micro-climate factors (Ritter et al., 2005; Zhu et al., 2007b; Albanesi et al., 2008; Latif and Blackburn, 2010; He et al., 2012), and consequently, influence the regeneration in gaps. Present studies have proposed that the photosynthetic active radiance (PAR) value mostly increases and is higher at the northern parts of gaps but is lower at the southern parts of gaps in the northern hemisphere (Zhang et al., 2001; Zhu et al., 2007b). It can be indicated that gap size and within-gap position are the direct “driving forces” for natural regeneration in forest gaps. For the sprout regeneration, it has been indicated that light can facilitate the growth of plant sprouts and can especially promote three growth traits: relative growth rate (RGR), total biomass, and leaf mass per unit area (LMA) (Rydberg, 2000; Kubo et al., 2005). These growth traits can reflect plant adaptability (Reich et al., 2003; Yan et al., 2016) and consequently, enhance seedlings’ adaptability in relation to environmental gradients (especially light irradiance levels) (Evans and Poorter, 2001; Jensen et al., 2012). However, little is known about the role of light in facilitating sprout regeneration in terms of photosynthesis. Photosynthesis, which is closely related to the changes in light, is one of the vital physiological processes for seedling growth (Kozlowski and Pallardy, 1997; Jensen et al., 2012). The chlorophyll concentration is an important determinant factor of the light-capturing ability of the leaf, and lower irradiance usually results in a lower chlorophyll content (Kramer and Kozlowski, 1979; Sun et al., 2016). The carotenoid content is closely correlated with light intensity and can protect chloroplasts from

2. Materials and methods 2.1. Study site The study was carried out at Daxicha (41°50′N, 124°47′E, elevation 600–800 m a.s.l.), 20 km away from Qingyuan Forest CERN, Chinese Academy of Sciences in Liaoning Province, Northeast China. The climate of this area is a continental monsoon type with a strong windy spring, a hot and humid summer and a dry and cold winter. The mean annual air temperature is 4.7 °C, and the extreme temperatures are 36.5 °C in July and −37.6 °C in January. The annual precipitation is 810.9 mm, of which 80% falls during summer from June to August. The frost-free period is approximately 130 days, and the growing season lasts from early April to late October (Yan et al., 2010). 2.2. Gap description The twelve artificial gaps used in this study were created randomly in typical secondary forests (dominated by Q. mongolica, A. mono and Fraxinus rhynchophylla). Gaps were created on snow-covered ground in March 2015 to reduce the disturbances on the forest floor during logging. We harvested all trees, including saplings and shrubs higher than 2 m to create gaps. All logging materials were removed from the gaps to create a uniform forest floor that only consisted of grasses. There were similar site conditions for these artificial gaps with similar soil types (brown forest soil containing 25.6% sand, 51.2% silt and 23.2% clay (Yang et al., 2013)), topographies (mountains with slope of 18–28°, slope aspect of 158–228°, and mid-slope position), and vegetation compositions, as well as the same history of forest management. The diameter at breast height (DBH) of border trees ranged from 20 to 35 cm. According to the size of each gap, the gap size was classified as: large gap of the size > 600 m2, medium gap of the size 300–600 m2, and small gap of the size < 300 m2. Four gaps for each size category, and the basic description of these twelve experimental gaps was shown in Table 1. 2.3. Experimental design A preliminary investigation of all tree stumps within gaps was conducted in 2015 after logging to ascertain the basic information (e.g., tree species, stump diameter and height, within-gap location). According to this investigation, we selected three tree species with varying levels of shade tolerance (shade intolerant species: Q. mongolica; intermediate shade tolerant species: A. mono; shade tolerant species: T. mandshurica) as subjects in the present study (Shi et al., 2006; Wu et al., 2013; Yan et al., 2016). Because of the limitation on the inherent positions of these tree stumps in gaps, our experimental stumps with sprouts of the three tree species were only chosen from five within-gap positions (subareas) (north, south, east, west and center) (Fig. 1) in large-medium gaps (476–984 m2) to test the effects of the within-gap position on sprout regeneration. To determine the within268

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experimental stump and labelled them as experimental sprouts at the beginning of experiment (i.e., in May 2016). These three selected sprouts in each stump were considered as a representative of the stump. Then we measured their photosynthesis, foliage traits and growth characteristics in each stump. At the end of our experiment (September 2016), at the north, south, east, west and center positions in largemedium gap and center in small gap, the numbers of sprout (mean ± S.D.) were 25.67 ± 28.11, 8.33 ± 5.69, 11.00 ± 3.00, 7.00 ± 4.24, 12.33 ± 0.58 and 18.00 ± 16.97 for Q. mongolica, and 10.00 ± 3.46, 10.33 ± 0.58, 11.00 ± 4.00, 8.00 ± 2.65, 11.67 ± 4.73 and 13.50 ± 4.95 for A. mono, and 11.00 ± 3.61, 16.67 ± 13.28, 13.00 ± 3.00, 18.67 ± 13.32, 17.00 ± 8.49 and 9.33 ± 6.03 for T. mandshurica, respectively.

Table 1 Basic description of twelve experimental forest gaps in the secondary forest. Experimental forest gaps

Gap size (m2)

Altitude (m)

Aspect (°)

Slope (°)

Height of gap border trees (m)

DBH of gap border trees (cm)

LG1 LG2 LG3 LG4 MG1 MG2 MG3 MG4 SG1 SG2 SG3 SG4

984 688 968 658 476 484 512 492 260 226 184 176

678 679 653 672 664 726 731 762 699 686 708 713

191 170 195 220 168 170 158 170 228 195 208 165

22 25 19 25 18 25 28 26 28 28 22 27

20 20 18 20 19 19 17 19 20 17 17 17

27.3 30.8 28.9 32.6 28.8 31.6 26.5 32.5 27.1 20.3 21.1 25.8

2.4. Photosynthesis The photosynthesis measurement was conducted in August 2016 by using a LI-6400 Portable Photosynthesis System (LI-COR, Inc., Lincoln, NE, USA) with a red-blue light-emitting diode light source (6400-02B) in an ambient environment on consecutive sunny days. The light response curves were measured between 9:00 and 12:00 on fully expanded leaves of the selected two-year-old stump sprouts of each experimental stump. The photosynthetic photon flux density (PPFD) was designed as follows: 2000, 1800, 1500, 1200, 1000, 800, 500, 200, 120, 80, 50, 20, and 0 μmol m-2 s-2. The light response curves were modeled using a rectangular hyperbolic model; then, the parameters, such as light-saturated net photosynthetic rate (PNmax) and dark respiration rate (Rd), were calculated directly (Singsaas et al., 2001; Gao et al., 2015).

Note: LG: Large gap; MG: Medium gap; SG: Small gap.

2.5. Foliage traits Foliage samples of the selected sprouts for photosynthesis measurement were collected in August 2016 to determine the leaf mass per unit area (LMA) and photosynthetic pigment content. LMA was calculated as follows:

Fig. 1. The sketch map of sampling area within experimental forest gaps.

gap position, we first confirmed the midpoint between the center point and the border tree (edge) of the gap. The center area of the gap (the blue1 area in Fig. 1) was identified as the circular area from the center point to the midpoints, with the radius of this circle of 6.16–8.85 m. The transition area (the white area in Fig. 1) was considered as the annular area from the midpoints to the edge points, and was divided into four subareas (north, south, east and west) with the northeast-southwest line and the southeast-northwest line across the center point. The concrete partition of five within-gap positions (subareas) was shown in Fig. 1. Furthermore, to explore the effects of gap size on regeneration, stumps with sprouts of the three tree species were only chosen from two gap sizes (large gaps and small gaps) at the same within-gap position (center). There were three replicates of stumps for each within-gap position and gap size treatment, and each replicate was selected from different gaps. In order to avoid the competition with other sprouts on the same stump, we just randomly chose each replicate of stump with common 10–30 sprouts for each treatment in May 2015. After measurement in May 2016, we calculated the mean stem height (Hm) and mean basal stem diameter (Dm) of the sprouts in each experimental stump. The stump height (mean ± S.D.) and stump diameter (mean ± S.D.) were 19.67 ± 9.51 cm, 21.50 ± 11.57 cm, 23.00 ± 9.83 cm and 19.80 ± 13.23 cm, 5.61 ± 2.06 cm, 8.47 ± 5.71 cm for Q. mongolica, A. mono and T. mandshurica, respectively. Then, we randomly selected three two-year-old stump sprouts with the height of Hm ± S.E. (standard error) and the basal diameter of Dm ± S.E. from each

LMA (g·m−2) = leaf mass/leaf area

(1)

2

where the leaf area (m ) is estimated with computer image analysis software (Díaz-Barradas et al., 2010) and leaf mass is the dry weight of each foliage sample after the foliage was dried at 65 °C for 72 h to a constant mass. The photosynthetic pigment content including the chlorophyll content (Chl) and carotenoid content (Car) was determined spectrophotometrically using 80% acetone extracts (Zhu et al., 2014). Each foliage sample was cut up and mixed well. Then 0.05 g of foliage sample was put into 10 ml of 80% acetone (v/v) and extracted avoiding light for 1–2 days. After complete extraction, we conducted the colorimetric analysis with spectrophotometer (UA1880, Jinghua Instruments, China) at the wavelength of 663 nm, 645 nm and 470 nm. Chla, Chlb and Car were calculated as follows:

Chla = (12.21A663 −2.81A645 ) × V/(M × 1000)

(2)

Chlb = (20. 13A645 −5. 03A663 ) × V/(M × 1000)

(3)

Car = ((1000A 470 −3.27Chla−104Chlb)/229) × V/(M × 1000)

(4)

where the A663, A645 and A470 are the values of absorbance at the wavelength of 663 nm, 645 nm and 470 nm, respectively. V is the volume of extract (ml), and M is the fresh weight of leaves (g). The total nitrogen (N) content of leaf samples (% dry mass) was determined by the elemental analyzer (Elementar Analysen Systeme GmbH, Germany). 2.6. Growth parameters

1

For interpretation of color in Fig. 1, the reader is referred to the web version of this article.

The initial basal diameter (D1) of the experimental stump sprouts 269

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five within-gap positions of three gap sizes and the photos were analyzed by Gap Light Analyzer (Version 2.0).

were measured at the beginning of the experiment (i.e., in May 2016). Samples of all three stump sprouts of each experimental stump were harvested at the end of our experiment (i.e., in September 2016). All stump sprouts were separated into two parts: leaves and stems. The final basal diameter (D2) of each harvested sprout was measured. All samples were killed at 105 °C for 30 min and then dried at 65 °C for 72 h to a constant mass in a drying oven. The dry weight of each part was determined with a laboratory electronic balance. Then, the aboveground biomass and the increment of basal diameter (IBD) during the growing season were calculated. The IBD (mm) was computed as follows:

2.8. Data analysis For each parameter of stump sprouts under the same within-gap position or gap size, the mean values of three replicates for each tree species with a level of shade tolerance were used for comparison. All data were tested for homogeneity of variance before any specific statistical procedures were performed. The photosynthetic characteristics, foliage traits, and growth parameters of sprouts may be influenced by random factors (i.e., sprouting ability of stump and site condition) and fixed factors (i.e., gap size and within-gap position). Because we took the number of sprouts per stump as the sprouting ability of stump and chose the stump with 10–30 sprouts as our experimental stump in May 2015 to minimize the difference of sprouting ability between stumps per tree species. Furthermore, to minimize the effect of site condition, we created twelve experimental forest gaps with similar terrain environment and similar gap characteristics in 2015 (Table 1). Thus, by using the means comparison analysis, the random effects of sprouting ability of stump and site condition were very small. Only within-gap position and gap size became the fixed factors which we should consider. The effects of within-gap positions on photosynthetic characteristics, foliage traits and growth parameters were tested using one-way ANOVA. Once the effect was significant, least significant difference (LSD)’s post hoc test was used to examine the differences among five within-gap positions for each tree species. An Independent-Samples ttest was used to distinguish between the two gap sizes (large and small gaps) for the photosynthetic characteristics, foliage traits, and growth parameters at the same position (center). The two-way ANOVA analysis was used to test the effect of within-gap position and gap size on canopy openness. Correlation analyses with a Pearson coefficient were

(5)

IBD = D2−D1

where D1 and D2 are the stem basal diameter at the beginning and end of the experiment, respectively. 2.7. Environmental condition monitoring For better understanding the variation of microclimate within gaps, we randomly selected one gap from each size of gap and set data loggers (WatchDog 1650 Micro Station, Spectrum Technologies) at five within-gap positions. The environmental conditions (including light availability, air temperature and relative humidity, soil water content and soil temperature) were continuously monitored with data loggers during the growing season (from May to September) in 2016. Light availability, defined as photosynthetically active radiance (PAR), was automatically monitored by a quantum light sensor (Spectrum Technologies. lnC, Item #36681) at a height of 1.0 m above the forest floor, and the soil temperature and soil water content were monitored at 5 cm below ground. The mean value of each environmental parameter during the observation was shown in Fig. 2. Moreover, we determined the canopy openness using the hemispherical photography at

30

Soil temperature (°C)

(A) PAR

400

-2

-1

)

500

300 200 100 0

Medium gap

(C) Soil water concent

24 16 8

Large gap

Medium gap

Air relative humidity (%)

Large gap

Medium gap

Small gap

Medium gap

Small gap

(D) Air temperature

24 18 12 6

Large gap

Gap size

(E) Air relative humidity

North South East West Center

80 60 40 20

Large gap

6

0

Small gap

100

0

12

30

32

0

18

0

Small gap

Air temperature (°C)

Soil water content (%)

40

Large gap

(B) Soil temperature

24

Medium gap

Gap size

Small gap

Fig. 2. The mean values of environment parameters in gaps during the growing season in 2016. 270

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the southern part of gaps (Q. mongolica: 4.92 μmol m-2 s-1, A. mono: 3.89 μmol m-2 s-1), but for the T. mandshurica stump sprouts, the minimum PNmax existed at the eastern part of gaps (Fig. 4A). For all three tree species, only the PNmax of Q. mongolica was significantly different among within-gap positions (P < 0.05); the PNmax at the southern and eastern parts were significantly lower than those in the west and center (P < 0.05) (Fig. 4A). The Rd values for stump sprouts of all tree species showed no significant differences among five withingap positions (P > 0.05) (Fig. 4B). At both the western and center parts of gaps, the PNmax of Q. mongolica was significantly higher than that of the other two tree species (P < 0.05) (Fig. 4A). However, at the southern part of gaps, the PNmax of T. mandshurica (10.26 μmol m-2 s-1) was significantly higher than those of Q. mongolica (4.92 μmol m-2 s-1) and A. mono (3.89 μmol m-2 s-1) (P < 0.05).

Table 2 Effects of gap size and within-gap position on canopy openness. Factor

Df

F-statistic

P-value

Gap size Within-gap position Gap size × within-gap position

2 4 8

19.34 0.64 0.37

< 0.001 0.637 0.933

conducted to test the relationship between PNmax and LMA for each tree species. All of the above analyses were performed using SPSS 20.0, and significance was examined at the level P < 0.05. 3. Results 3.1. Environmental conditions

3.3. Foliage traits

The variation of soil temperature, air temperature and air relative humidity were not obvious among within-gap positions or gap sizes (Fig. 2B, D, E). The maximum PAR occurred at the northern part of the large and small gaps and the center part of the medium gaps, respectively. The minimum PAR occurred at the southern part of all three sizes of gaps (Fig. 2A). The values of PAR increased with the increasing gap size (Fig. 2A). The values of soil water content at the west part and center of gaps were higher than the other three within-gap positions (Fig. 2C). The gap size and within-gap position did not show the interactive effect on the canopy openness (P > 0.05) (Table 2). Only the gap size could significantly affect the canopy openness (P < 0.05) (Table 2), and the canopy openness increased with the gap size (Fig. 3).

Gap sizes had no significant effects on the Chl, Car and Chl a/b of stump sprouts for all three tree species (P > 0.05) (Fig. 5A–C). Only the LMA of Q. mongolica showed a significant difference between large gaps (78.54 μmol m-2 s-1) and small gaps (55.14 μmol m-2 s-1) (P < 0.05) (Fig. 5D). In both large gaps and small gaps, the LMA of Q. mongolica was significantly higher than that of A. mono and T. mandshurica (P < 0.05) (Fig. 5D) and the Chl and Car of T. mandshurica were significantly lower than those of Q. mongolica and A. mono (P < 0.05) (Fig. 5A, B). No foliage variables were significantly influenced by the within-gap position for the stump sprouts of all three tree species (P > 0.05) (Fig. 6). The Chl and Car of Q. mongolica and A. mono sprouts were significantly higher than those of T. mandshurica at the same within-gap position, except for the northern part of gaps (P < 0.05) (Fig. 6A, B). The Chl a/b of Q. mongolica sprouts was significantly higher than A. mono at the southern, eastern and center parts of gaps (P < 0.05) (Fig. 6C). The LMA of Q. mongolica was significantly higher than that of A. mono and T. mandshurica at all within-gap positions, excepting the LMA of A. mono at the northern and western parts of gaps and the LMA of T. mandshurica at the western part of gaps (P < 0.05) (Fig. 6D). For all three tree species, there was no significant correlations between PNmax and LMA (P > 0.05) (Table 3). Gap size had no significant effect on the N concentration in leaves of stump sprouts for all three tree species (P > 0.05) (Fig. 7B). Only N concentration in leaves of stump sprouts of A. mono was significantly influenced by the within-gap position, i.e., the N concentration in leaves of A. mono at the center part of gaps was significantly higher than that at the south part of gaps.

3.2. Photosynthetic response The PNmax and Rd of Q. mongolica stump sprouts in large gaps (PNmax: 26.49 μmol m-2 s-1, Rd: 2.3 μmol m-2 s-1) were significantly higher than those in small gaps (PNmax: 8.78 μmol m-2 s-1, Rd: 1.32 μmol m-2 s-1) (P < 0.05), but the PNmax and Rd values for the stump sprouts of the other two tree species were not significantly different between large gaps and small gaps (P > 0.05) (Fig. 4C, D). In small gaps, the Rd of A. mono (0.42 μmol m-2 s-1) was significantly three times lower than that of Q. mongolica (1.32 μmol m-2 s-1) or T. mandshurica (1.50 μmol m-2 s-1) (P < 0.05) (Fig. 4D). The maximum value of PNmax occurred at the center of gaps for the stump sprouts of all three tree species (Q. mongolica: 26.49 μmol m-2 s-1, A. mono: 6.91 μmol m-2 s-1, T. mandshurica: 14.46 μmol m-2 s-1) (Fig. 4A). The minimum PNmax of Q. mongolica and A. mono occurred at 35

28

Canopy openness (%)

3.4. Growth parameters

Large gap Medium gap Small gap

The increment of basal diameter (IBD) of all three tree species was not significantly different among within-gap positions and gap sizes (P > 0.05) (Fig. 8A, B). The leaf dry biomass, stem dry biomass and aboveground biomass of Q. mongolica and A. mono in large gaps were significantly higher than those in small gaps (P < 0.05), but all the three parameters of T. mandshurica exhibited no significant difference between large gaps and small gaps (P > 0.05) (Fig. 9D–F). The leaf dry biomass of stump sprouts in large gaps showed significant difference among the tree species (Q. mongolica: 40.06 g, A. mono: 27.69 g, T. mandshurica: 7.82 g) (P < 0.05) (Fig. 9D). The aboveground biomass of Q. mongolica (178.91 g) and A. mono (158.42 g) in large gaps were significantly higher than that of T. mandshurica (46.54 g) (P < 0.05) (Fig. 9F). All three parameters showed no significant differences among the tree species in small gaps (P > 0.05) (Fig. 9D–F). The within-gap position had no significant effect on leaf dry biomass, stem dry biomass and aboveground biomass of Q. mongolica and T. mandshurica (P > 0.05) (Fig. 9A–C), but these three parameters exhibited significant differences in A. mono stump sprouts among the

21

14

7

0

North

South

East

West

Center

Within-gap position Fig. 3. Canopy openness at five within-gap positions under three different sizes of gaps. 271

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35 (A)

aA

aA

25

(B)

aA )

-1

aB

PNmax

15

bA

10

aA

bB 5 0

Q.mongolica

aAaB aB aB A.mono

1.5

aB aAaA aA

0.0

T.mandshurica Large gap Small gap

aA

Q.mongolica

A.mono

T.mandshurica

(D)

)

2.5

aA aA aA

-1 -2

20

aA

2.0

aB bA

10

aA

aA

bA

1.5

Rd

)

-1 -2

PNmax

aA aA

0.5

25

aB

1.0

aB 0.5

5 0

aA

aA aA aA

3.0 (C)

15

aA aA

1.0

35 30

aAaA

2.0

-2

abA

aA

aA

Rd

-2

20

aAaA

2.5

-1

)

30

3.0

North South East West Center

Q.mongolica

A.mono

0.0

T.mandshurica

Q.mongolica

Tree species

A.mono

T.mandshurica

Tree species

Fig. 4. Light-saturated photosynthetic rate (PNmax) and dark respiration rate (Rd) in the leaves of stump sprouts of three broadleaved tree species at different withingap positions (A, B) or gap sizes (C, D). Capital letters above the column represent a significant difference at P < 0.05 among the three tree species. Lowercase letters above the column indicate a significant difference at P < 0.05 among five within-gap positions or two gap sizes. The values are the means ± S.E. of the three replicated stump sprouts. 8 7

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Fig. 5. Comparison of foliage traits of stump sprouts of three tree species of varying levels of shade tolerance in two sizes of gaps. Capital letters represent a significant difference at P < 0.05 among three tree species at the same gap size. Lowercase letters indicate a significant difference at P < 0.05 between large gaps and small gaps for the same tree species. The values are the means ± S.E. of the three replicated stump sprouts.

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8

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Fig. 6. Comparison of foliage traits of stump sprouts of three tree species of varying levels of shade tolerance at five within-gap positions. Capital letters represent a significant difference at P < 0.05 among three tree species at the same within-gap position. Lowercase letters indicate a significant difference at P < 0.05 among five within-gap positions for the same tree species. The values are the means ± S.E. of the three replicated stump sprouts.

stump sprouts (Fig. 9A), but the minimum values of stem (39.13 g) and aboveground biomass (53.07 g) occurred at the southern part of gaps (Fig. 9B, C). At the eastern and center parts of gaps, the leaf, stem and aboveground biomass of Q. mongolica were significantly higher than those of T. mandshurica (P < 0.05) (Fig. 9A–C).

Table 3 The relationship between PNmax and LMA for three tree species in 2016. r refers to Pearson correlation coefficient; Significance was examined at the level Pvalue < 0.05. Tree species

r

P-value

Q. mongolica A. mono T. mandshurica

0.210 −0.214 0.591

0.690 0.684 0.217

4. Discussion 4.1. Effects of gaps on light environment

five within-gap positions (P > 0.05) (Fig. 9A–C). The maximum values of leaf dry biomass (27.69 g), stem dry biomass (130.73 g) and aboveground biomass (158.42 g) occurred at the center part of gaps for A. mono stump sprouts (Fig. 9A–C). The minimum value of aboveground biomass (11.15 g) occurred at the western part of gaps for A. mono

Studies have shown that forest gaps affect the micro-environmental conditions and consequently influence plant regeneration (Mcalpine and Drake, 2002; Zhu et al., 2003; Albanesi et al., 2008). The formation of a gap results in changes in the light environment, and the light intensity (PAR) varies dramatically in different within-gap positions and

5

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N concentration (%)

N concentration (%)

West aA

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A. mono Tree speceis

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0

Q. mongolica

A. mono Tree species

273

T. mandshurica

Fig. 7. Comparison of N concentration in leaves of stump sprouts of three tree species of varying levels of shade tolerance at five within-gap positions (A) and under two gap sizes (B). Capital letters represent a significant difference at P < 0.05 among three tree species at the same within-gap position or gap size. Lowercase letters indicate a significant difference at P < 0.05 among five within-gap positions or two gap sizes for the same tree species. The values are the means ± S.D. of the three replicated stump sprouts.

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10

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Increment of basal diameter (mm)

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0 Q.mongolica

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Fig. 8. Increment of basal diameter of stump sprouts of three tree species at five within-gap positions (A) or in two sizes of gaps (B) during the study period. The values are the means ± S.E. of the three replicated stump sprouts.

Stem dry biomass (g)

North South East West Center

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Stem dry biomass (g)

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70

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aA

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T.mandshurica

Tree species

200

(F) aA aA

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bA

Q.mongolica

bA

A.mono

aA aB

T.mandshurica

Tree species

Fig. 9. Biomass of stump sprouts of three tree species at five within-gap positions (A, B, C) or two gap sizes (D, E, F) at the end of the experiment. A and D show the leaf dry biomass, B and E show the stem dry biomass, and C and F indicate the aboveground biomass. Capital letters represent a significant difference at P < 0.05 among the three tree species at the same within-gap position or gap size. Lowercase letters indicate the significant difference at P < 0.05 among different within-gap positions or gap sizes for the same tree species. The values are the means ± S.E. of the three replicated stump sprouts. 274

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4.3. Effects of gaps on foliage traits

gap sizes (Clinton, 2003; Ritter et al., 2005). Previous studies have proposed that the value of PAR increases significantly with gap size (De Freitas and Enright, 1995; Latif and Blackburn, 2010). Our results were in agreement with these studies, i.e., the average value of PAR in small gaps was lower than in the other two gap sizes (Fig. 2A). Zhang et al. (2001) proposed that the PAR value mostly increased at the northern part of gaps in the northern hemisphere, and Zhu et al. (2007b) indicated that the highest PAR value occurred at the northern edge of the gap. Our results led to similar conclusions in large and small gaps. The average PAR value was higher at the northern part of gaps and lowest at the southern part of gaps, which might be affected by the location in the northern hemisphere (Zhu et al., 2007b).

Chl is a major determinant that reflects the plant photosynthetic ability (Du et al., 2009); a lower Chl is usually the result of plants growing under a weaker light condition for a period of time. However, in our study, neither the within-gap position nor gap size had significant effects on the Chl of stump sprouts of any of the tree species. Car is important for plants in high light environments to protect chloroplasts against damage from high irradiance (He et al., 2010), and variations in the Chla/b values and Car content are correlated with plant adaptability (Wang et al., 2011). In the present study, we found that variations in Car and Chla/b for the stump sprouts of three tree species among within-gap positions and gap sizes was similar to the variation in Chl, i.e., the within-gap position and gap size did not influence Car and Chla/b. These results implied that at the early stage of gap formation, changes in environmental factors within gaps or between two gap sizes had a smaller impact on the photosynthetic pigments of stump sprouts of tree species of varying levels of shade tolerance. We also found that the concentrations of photosynthetic pigments of Q. mongolica and A. mono were significantly higher than those of T. mandshurica. This finding indicated that, compared with the stump sprouts of T. mandshurica (shade tolerant tree species), stump sprouts of Q. mongolica (shade intolerant tree species) and A. mono (intermediate shade tolerant tree species) in gaps had better adaptability to the changing environmental conditions. Stump sprouts of these tree species exhibited a plasticity in the leaf morphological trait (LMA) in response to light irradiance. This trait would be beneficial for seedlings to survive for a long period in the understory (Reich et al., 2000; Pollastrini et al., 2011). LMA is also a feature of shade acclimation in many tree species among seedlings growing under different light environments; a greater photosynthetic capacity is related to a higher LMA (Ellsworth and Reich, 1992; Evans and Poorter, 2001; Pollastrini et al., 2011; Jensen et al., 2012). We found that most of the LMA in the leaves of Q. mongolica stump sprouts were significantly higher than those in the other two tree species. This result indicates that the photosynthetic capacity of Q. mongolica stump sprouts is the greatest among the selected tree species in the forest gaps. A reduction in LMA is a typical shade acclimation response (Sun et al., 2016), but this is not completely consistent with our results. In our study, gap size only showed a significant influence on the LMA of Q. mongolica, and the within-gap position showed no significant effect on the LMA of all three tree species. These differences might be explained by the fact that at the early stage of gap formation, the LMA of tree species is affected by the interactive effects of tree stumps and natural environments on nutrients supply (including macronutrients (e.g., carbon, nitrogen, phosphorus, potassium, calcium and magnesium) and micronutrients (e.g., copper and zinc)) (Iwasa and Kubo, 1997; Zhu et al., 2007c). Nitrogen (N) is considered as an essentially limiting factor for plant growth in many ecosystems (Shi et al., 2015). Moreover, the leaf N can also be considered as a determinant of photosynthetic capacity (Takashima et al., 2004). However, in our study, the leaf N concentration showed significant differences among five within-gap positions for the A. mono, but the photosynthesis rate of A. mono was not significantly affected by the within-gap positions. This inconsistency may be because of the trade-off in leaf N partitioning of stump sprouts for each tree species between investing in photosynthesis and persistence (Takashima et al., 2004).

4.2. Effects of gaps on photosynthetic responses Photosynthesis is one of the most important physiological processes for tree growth (Jensen et al., 2012; Sun et al., 2016). Stump sprouts acclimate to different light environments by adjusting their photosynthetic characteristics (PNmax and Rd). In the present study, we found various patterns for tree species of varying levels of shade tolerance to adjust to varying light environments. Only Q. mongolica stump sprouts showed a significant difference in photosynthetic parameters between large gaps and small gaps. These results were partly consistent with the previous research of Albanesi et al. (2008), in which the PNmax values for silver fir seedlings regenerated from seeds were significantly different between medium gaps and small gaps. This may be because stump sprouts can obtain nutrients (including macronutrients (e.g., carbon, nitrogen, phosphorus, potassium, calcium and magnesium) and micronutrients (e.g., copper and zinc)) not only from the natural environment but also from tree stumps (Iwasa and Kubo, 1997; Zhu et al., 2007c). Therefore, even stump sprouts growing in small gaps with the lowest light availability were able to obtain enough nutrients from stumps. The within-gap position had significant effects on the PNmax of only Q. mongolica stump sprouts, and the PNmax values were significantly higher at the western and central parts of gaps than those at the southern and eastern parts of gaps. The results indicated that as a shade intolerant tree species, photosynthesis of Q. mongolica stump sprouts was much more easily affected by the within-gap position and that the moderate light environment at the western and central parts of gaps may be more beneficial to its photosynthesis. Though the value of PAR at the northern part of gaps was higher than at other positions within gaps, the PNmax of Q. mongolica stump sprouts at this location was relatively low. The variation of Rd for Q. mongolica stump sprouts was consistent with PNmax among different within-gap positions, though the variation was not statistically significant. The lower Rd values at the southern and eastern parts of gaps can be explained as a strategy for energy conservation by seedlings to decrease the respiratory loss of CO2 and create a positive carbon balance under low light conditions (Zhu et al., 2014). These results implied that the western and central parts of gaps might be more beneficial for Q. mongolica stump sprouts to accumulate biomass, but on the contrary, the southern and eastern parts of the gaps might be adverse for the sprouts to accumulate biomass. The PNmax of Q. mongolica and A. mono stump sprouts were significantly lower than those of T. mandshurica under the weak light condition (the southern part of gaps), but under the moderate light condition (the western and central parts of gaps), the PNmax of Q. mongolica was significantly higher than that of A. mono and T. mandshurica. The Rd of stump sprouts at the same within-gap position showed no significant differences among tree species. These results indicated that Q. mongolica (shade intolerant tree species) might accumulate less biomass than T. mandshurica (shade tolerant tree species) under weak light conditions, but compared with T. mandshurica, the moderate light condition within gaps might be more benefit to biomass accumulation in Q. mongolica.

4.4. Effects of gaps on growth of stump sprouts Plants with a high PNmax and low Rd generally have a strategy of energy conservation to accumulate more biomass. However, this rule is not suitable for our study. In our study, the increment of basal diameter of all three tree species was not significantly different among gap sizes or within-gap positions. The gap size had a significant influence on the 275

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locate the stumps of Q. mongolica in the western of a gap, the Q. mongolica trees can be felled as the western position of a gap, and the gap can be created towards the east (Fig. 10B). It can be concluded that this study has provided new insights for improving the directed cultivation and restoration of Q. mongolica in secondary forests. 5. Conclusions The within-gap position and gap size had significant effects on the photosynthetic characteristics of stump sprouts of only Q. mongolica (shade intolerant tree species). For the influence of within-gap position, the moderate light condition at the western and central parts of gaps might be more beneficial to its photosynthesis; on the contrary, the weak light condition at the southern and eastern parts of gaps might be adverse to sprout photosynthesis; for the effect of gap size, we found that the photosynthesis ability of Q. mongolica in the large gap was much higher than that in the small gap. Forest gaps had a smaller impact on the photosynthetic pigments of stump sprouts of tree species with varying levels of shade tolerance. Gap size could significantly affect the biomass of stump sprouts of both Q. mongolica and A. mono (intermediate shade tolerant tree species). However, within-gap position only had remarkable effect on the biomass of stump sprouts of A. mono. It can be concluded that the influence of forest gaps on the growth of stump sprouts were not consistent with their photosynthetic responses, which is because stump sprouts could obtain enough nutrients to maintain their growth not only from environment but also from their stumps or roots. Once the gap formation, stump sprouts of Q. mongolica and A. mono showed a better adaptability than T. mandshurica (shade tolerant tree species) to the changing habitat environment caused by the forest gap. Based on these findings, we can provide some forestry applications in forest management. For example, creating a large gap with the Q. mongolica stump located in the center or western position of the gap is more beneficial to its stump sprout regeneration. Our study only presents the general characteristics of sprout regeneration at the early stage of gap formation, and the growth of stump sprouts still needs to be continuously monitored to explore the longterm effects of gaps.

Fig. 10. The sketch map of forestry application in promoting the sprout regeneration of Quercus mongolica by creating a gap. (A) logging the Q. mongolica trees and locating them as the gap center area; (B) logging the Q. mongolica trees and locating them as the western position of a gap.

biomass of Q. mongolica and A. mono stump sprouts, and the within-gap position had a significant effect on the biomass of only A. mono stump sprouts. However, as mentioned above, the within-gap position and gap size only showed significant effects on the photosynthetic characteristics of Q. mongolica. At the early stage of gap formation, sprouts regenerated from stump could obtain nutrients from both soil and the stumps, which maybe lead to the inconsistency between photosynthetic responses and growth in our study (Iwasa and Kubo, 1997; Zhu et al., 2007c). Thus, the effect of gap environment on the growth of stump sprouts may be not as significant as expected.

Funding This research was supported by grants from the National Natural Science Foundation of China (31330016, 31670637) and the Youth Innovation Promotion Association CAS (2011158). References

4.5. Forestry application based on gap formation

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Among the three selected tree species with contrasting shade tolerance, we took Quercus mongolica as an example to indicate the forestry application based on this study. Q. mongolica, one of the dominant broadleaved tree species in the natural secondary forests in northeast China (Wang et al., 2008), has poor regeneration performance (Zhang, 2013). Therefore, many efforts had been made to promote their seed regeneration (Yan et al., 2010, 2012). As an effective form of regeneration, however, stump sprouting of oak species often occur after gap formation, and some studies had indicated that creating a gap in the forest was beneficial to the sprout regeneration of woody plants (e.g., oak species) (Morrissey et al., 2008; Atwood et al., 2009). To promote the photosynthesis and growth of the stump sprout of Q. mongolica based on our findings, we can control the gap size (i.e., large gap) and the within-gap position (i.e., at the center or the western position) of its stump sprout during the gap formation. Therefore in the forestry application, if we want to locate the stumps of Q. mongolica in the center of a gap, the Q. mongolica trees can be logged as the gap center area to create a large gap (Fig. 10A). Furthermore, if we want to 276

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