Photosynthesis adaption in Korean pine to gap size and position within Populus davidiana forests in Xiaoxing’anling，China

Xuannan Li·Yahui Wang·Zhihui Yang·Ting Liu·Changcheng Mu

Abstract Forest gaps restrict the restoration of temperate secondary forest to broad-leaved Korean pine forest in zonal climax vegetation by affecting the growth of Korean pine(Pinus koraiensis).However，the photosynthetic adaptability of Korean pine to gap size and position within the gap is unclear.In order to explore the adaptability of young Korean pine (35 years) to different gap sizes in Xiaoxing’anling，photosynthetic capacity and microenvironmental factors(leaf temperature，light transmittance) of Korean pine needles in three positions in the gap (central，transition，and edge areas) were investigated.Three gaps were identified in the secondary Populus davidiana forest:a large 201 m2 gap，a middle 112 m2 gap，and a small 50 m2 gap;12 m2 of the understory was sampled as a control.The results show that:(1) maximum net photosynthetic rate (P max) in needles of Korean pine growing in the large gap was higher than in the small gap，and Pmax in the centre in the same gap was higher than in the transition and edge areas;(2) light saturation point (LSP) and photosynthetic quantum yield (AQY)of needles in the large gap were higher than in the small gap，while the light compensation point (LCP) and chlorophyll contents of needles were lower in the small gap;and，(3)Pmax had a significant positive correlation with temperature and light transmittance.It is suggested that the larger the gap in secondary Populus davidiana forests，the greater the change in light intensity and temperatures，the stronger the light adaption of Korean pine needles and the higher the photosynthetic capacity.Therefore，in the recovery of broadleaved/Korean pine forests，suitable gaps should be created and gap microhabitats fully utilized to accelerate the restoration process.

Keywords Pinus koraiensis ·Gap size·Position in the gap·Maximum net photosynthetic rate

Introduction

Korean pine (Pinus koraiensisSiebold &Zucc.) is the most important and dominant tree species in natural broad-leaved Korean pine forests.It is also the foundation species of the climax forest type in northeast China，a national II-level protected wild species and one of the most valuable timber species (Nie et al.2008).It is distributed in parts of Russia，North Korea，Japan and the northeast from Xiaoxing’an to Changbai Mountain in China (Nie et al.2008).It has an important role in maintaining forest ecological functions and in sustainable economic development (Li 2 007).Broadleaved Korean pine (Pinus koraiensis) forest is the zonal climax vegetation in the eastern mountainous area of northeast in China.Due to long-term harvesting，most of the pine forests have degraded into broad-leaved secondary forests.Planting Korean pine under the secondary forest canopy is an effective way to restore the broad-leaved Korean pine forest.However，pine productivity is low due to the limitation of light by this method (Zhu et al.2014).

Light intensity is a major environmental factor affecting plant growth and distribution (Tang et al.2015)，and restricts plant photosynthesis (Granata et al.2020;Hu et al.2020).The growth of Korean pine saplings requires a lowlight environment，which has the characteristics of shadetolerant plants，but the amount of light required gradually increases with age (Pulinets 1986;Li 1998).Studies have shown that 3-year-old and 5-year-old Korean pine grow better under 30% to 60% of full light，7-year-old saplings grow best under full light (Sun et al.2009)，and 29-yearold trees have increased photosynthetic pigment content and enhanced photosynthetic capacity under high intensity light transmission (10 m diameter direct light transmission) (Yu et al.2014).However，it is still unclear whether the photosynthetic capacity of Korean pine in a forest increases with increase in light intensity after 29 years.

Gaps are the main form of disruption for many types of forests worldwide (Denslow 1987).They directly change the availability and spatial distribution of light by affecting the canopy structure，play an important role in survival and growth，regeneration and community succession of plants(Gray and Spies 1996;Whitmore 1989;Nicotra and Iriarte 1999;Mccarthy 2001).The size of the gap and the position within the gap are key characteristics which affect regeneration by changing the microenvironment (Zhang et al.2018).In recent years，research on photosynthesis of trees in gaps has become important.There are numerous studies on tree species in tropical regions (Andrew et al.2017;Costa et al.2019;Pang et al.2020;Santos and Ferreira 2020)，and less in temperate regions (Ater et al.2014;Riichi et al.2017)，and more research on associated tree species (Zhang et al.2018;Dumais et al.2020;Zhang and Yi 2021)，but less on dominant or endangered species(He et al.2019，2020).The photosynthetic characteristics of leaves essentially reflect the response mechanism by forest trees to the light environment(Santos and Ferreira 2020).At present，research on the physiological and ecological aspects of photosynthesis of Korean pine mainly involves drought stress (Zhang et al.2016)，edge effects (Wang et al.2003)，different light conditions (Zhou et al.2004;Sun et al.2009;Yu et al.2014) and leaf age(Huo and Wang 2007;Huang et al.2014;Zhu et al.2014)，while the impact of gaps on photosynthesis of Korean pine has not been reported.Maximum photosynthetic rate (Pmax)of 15-year-old Korean pine saplings in temperate broadleaved/Korean pine forests first increased and then decreased with the increase in gap size (Wang and Fan 2 009).Most of the previous studies were carried out in greenhouses or in artificial climate chambers，and most used seedlings as experimental materials;there are few studies on large trees in the natural state (Huang et al.2014;Liang and Liu 2019).Zang et al.(1999) noted that the regeneration density of Korean pine varies significantly with the age of the gap and the valley point period is within the gap development stage of 20-40 years，and so the regeneration and growth of young trees in this period is particularly important.In addition，Orman et al.(2018) reported that gap disturbance had different effects on species at different development stages，and its impact on young trees (height ＞ 1.3 m and diameter at breast height ≤5 cm) is stronger than on seedlings.For this reason and based on previous studies，in this study，young Korean pine (35-years-old) in aPopulus davidiana-Korean pine forest in the Xiaoxing’an Mountains in the temperate zone of northeast China were selected.Photosynthetic variables，chlorophyll content and microenvironment parameters of Korean pine needles in forest gaps of different sizes and different positions in the gap were measured to reveal the photosynthetic adaptability of 35-year-old pine to different gaps and to analyze the mechanisms and differences.The results may provide a basis for the regeneration，restoration and sustainable management of Korean pine in natural secondary forests.

Materials and methods

Overview of the study area

The study area site is located in Linban 353 (47°0′50″N，129°09′48″E) of the Daqingchuan Forestry Farm of the Dailing Forestry Experimental Bureau in Xiaoxing’an Forest Region，Heilongjiang Province.The region has a temperate continental humid monsoon climate，500-800 m a.s.l.Annual average temperature is 1.4°C，annual average rainfall 661 mm，mostly concentrated in July to September，and the frost-free period is about 115 days.The soil is a dark brown type and the vegetation a temperate coniferous and broad-leaved mixed forest with Korean pine as the community building species.Over several years，the forest has degenerated to various types of secondary forests withQuercus mongolica，Populus davidianaandBetula platyphyllaand other broadleaved species，and plantations.In the 1980s，the forest farm carried out an experiment to restore the Korean pine forest under aP.davidianaandB.platyphyllasecondary canopy.The density of 2-year-old pine was 3300 trees/ha and different intensities of light felling (shelterwood cutting) were carried out in 1989 (the harvest intensity ratio was 1/7-1/4).The tree layer of the site includedB.platyphylla，P.davidiana，F(xiàn)raxinus mandshurica andTilia amurensis.The shrub layer includedCorylus manshurica，Eleutherococcus senticosus，andSorbaria sorbifoliaand the herb layer consisted ofEriophorum vaginatumandCalamagrostis angustifolia.When the survey was conducted in 2019，the Korean pine was 35-years-old;the liberation cutting was at 30 years-of-age.A mixed coniferous and broad-leaved forest with different ages was initially formed.

Plant material

Young (35-year-old) pine in thePopulus davidiana-Korean pine forest were selected.Field experiments were carried out from May to October 2019 (growing season).The gaps are generally elliptical.According to the ratio (d/h)＜1.0 of the optimal gap diameter to the surrounding highest tree height required for the growth of shade tolerant tree species (Malcolm et al.2001)，three different gaps were selected:large，middle，and small gaps;an area without gaps was used as control.The semi-major axis (d/2) of gaps were about 8，6，4 and 2 m，and the gap size 201，112，50，and 12 m2，respectively.Trees in gaps were subdivided into three positions:the central area，the transition area and the edge，i.e.，d/2 was divided into three equal parts.The central area is the canopy gap，the transition area the area between the canopy gap and the expanded gap，and the edge area is the transition between the expanded gap and the area without gaps.The schematic diagram of the sample plot is shown in Fig.1.With the junction of the long and short axes as the gap center，the number，height and diameter at breast height (DBH) of tree species in the gap were recorded.There were three repeated plots in each gap and forest understory，for a total of 12 plots;each plot was located in the middle of the southwest slope，other site conditions remained the same.One sample tree was selected in the central area，transitional area，and edge area of each gap plot and forest plot.The total sample trees was 36 with three repetitions，and photosynthetic parameters，chlorophyll content，and microenvironmental factors of the needles measured.The specific conditions of the sample plot are shown in Table 1.

Table 1 Basic characteristics of the sample plots

Fig.1 Schematic diagram of sample plot

Determination of photosynthetic parameters

Photosynthetic parameters were measured during the 2019 growing season (May-October) once a month using a CIRAS-2 portable photosynthesis instrument (PP Systems Company，England) from 8:00 to 11:00 a.m.for a total of six measurements under clear，cloudless conditions.Needles in the middle of the canopy can use weaker or stronger light than needles in the top and bottom of the canopy (Huo and Wang 2007).Based on Zhang et al.(2006)，30-cm-long branches of Korean pine with good growth from the middle of the crown were inserted into water to prevent water loss and brought back to room temperature to determine photosynthetic parameters.Temperature and humidity were external parameters at the time of measurement.Illumination was provided by a LED light source in the assimilation chamber;photon flux density was set to 0，50，100，200 μmol·m-2·s-1，started from 200 μmol·m-2·s-1and increased by 200 μmol·m-2·s-1until 2000 μmol·m-2·s-1，and the photosynthetic parameters under each light intensity were recorded，including net photosynthetic rate (Pn)，transpiration rate (Tr)，stomatal conductance(Gs)，intercellular CO2concentration (Ci) and leaf temperature(TL).Water use efficiency (WUE) was calculated as

Light response curves under different forest gaps were measured andPmax，light compensation point (LCP)，light saturation point (LSP)，dark respiration rate (Rd) and AQY were calculated according to Farquhar et al.(1980).

Determination of light transmittance

For each forest gap，and before collecting needles，a Nikon CoolPix 4500 digital camera with 180° fisheye lens was used to collect three hemispherical pictures once a month in each gap.Using digital hemispherical photography 4.5.2 software to process hemispherical images，the canopy photographs were divided into three concentric rings relative to the gap center，transition area and edge，and the ratio of the canopy gaps in each ring was calculated to light transmittance.Because the shape of the gap was similar to an ellipse，the following were calculated:Clinton et al.1993

whereS(in m2) is the area of the gap，L(in m) is the length of the major gap axis，andW(in m) the length of the longest axis perpendicular to it;Scis the circle light transmission area，F(xiàn)gthe forest gap fraction;Tis the ring light transmission rate，Slthe ring light transmission area andSrthe ring area.

Determination of chlorophyll content

The harvested needles were sealed，placed into an ice bag and kept in an incubator (0-4°C) to be later brought back to the laboratory for chlorophyll extraction.Measurements were made in triplicate and included contents of chlorophyll a，chlorophyll b，total chlorophyll and the ratio chlorophyll a/b.Needles were kept in 20 mL 80% acetone for 24 h in the dark，and the chlorophyll concentration of the extract was measured according to (Arnon 1949).Measurements were taken once a month.

Data analysis

Statistical analysis was done using Excel (2010，Microsoft Corp.，USA) and SPSS (19.0，IBM Corp.，USA).Data shown in graphs are the means±standard deviation (SD)of three replicates.One-way ANOVA and least significant difference (LSD) tests were used to compare the differences between different data groups (α=0.05).The correlation betweenPmaxand other photosynthetic parameters and environmental factors was done through stepwise multiple linear regression，and the chart was drawn using SigmaPlot 14.0.

Results

Photosynthetic parameters of Korean pine needles under different sizes of gaps

The size of the gap had different effects on photosynthetic parameters (Fig.2).Values ofPmaxin the central and transition areas of the large gap were significantly higher than those in the middle gap by 21.8-21.9% (P＜0.05)，and in the central，transition and marginal zones they were also significantly higher than those in the small gap and in the forest，51.4-53.0% and 19.5-98.7%，respectively.Pmaxvalues in the central，transition and edge areas of the middle gap were significantly higher than those in the small gap and understory by 24.3-40.3% and 10.7-63.0%，respectively.There was no significant difference between each position in the small forest gap and in the understory (P＞ 0.05) (Fig.2 A).Therefore，Pmaxof Korean pine needles increased with increasing gap size at the central and transition areas (large gap ＞ middle gap ＞ small gap=forest)，yet it showed different trends at edge areas (large gap=middle gap ＞ small gap=forest).

Fig.2 Photosynthetic parameters of needles of Korean pine in different gap sizes.Notes Pmax:maximum net photosynthetic rate (A);LSP:light saturation point (B);LCP:light compensation point (C);AQY:apparent quantum yield (D);Tr:transpiration rate (E); Gs:stomatal conductance (F);WUE:water use efficiency (G); Rd:dark res-piration rate (H); Ci:intercellular CO2 concentration (I);CA:central area;TA:transition area;EA:edge area.Different lowercase letters indicate significant differences between gaps of different sizes，and different capital letters indicate significant differences between position (P＜0.05)

The effect of gap size on LSP of Korean pine needles was similar to the effect onPmax(Fig.2 B).LSP also increased with gap size in the central and transition areas，and in the large and middle gaps in the edge area was significantly higher than in the small gaps and the understory.However，the LCP in the central and transition areas of the large，medium and small gaps was significantly lower than in the understory and in the edge area;only the LCP of the large gap was significantly lower than that in the understory(Fig.2 C).The Rdin the central，transition and edge areas of all gaps (except for the edge of the small gap) was significantly lower than that in the understory (Fig.2 H).

Gap size also had a significant effect on the AQY，Tr and Gs(P＜0.05;Fig.2 D，E，F(xiàn))，but had no significant effect(P＞ 0.05) on either WUE or Ci(Fig.2 G，I).Values of AQY were significantly higher in the central and transitional areas of large gaps relative to same areas in small gaps and in theunderstory，and were significantly higher than those in middle and small gaps in the edge areas.AQY in the central area of the middle gap was significantly higher than those in the small gap and the understory，and in the transition area，it was only significantly higher than in the understory.In the small gap，AQY was significantly higher only in the central area than in the understory (Fig.2 D).Tr in the central and transition areas of the large gap was significantly higher than in the small gap and the understory，and in the central area of the middle gap，it was significantly higher than in the understory (Fig.2 E).Gswas significantly higher in the central and transition areas of the large gap than in the small gap and the understory，and significantly higher in the edge area of the middle gap than that in the small gap (Fig.2 F).Therefore，LSP was highest and LCP lowest in the central，transition and edge areas of the large gap.AQY，Tr and Gswere highest in the central and transition areas.

Gap size had a signif ciant effect (P＜0.05) on chlorophyll a，chlorophyll b，total chlorophyll contents and chlorophyll a/b levels (Fig.3).Chlorophyll a，chlorophyll b and total chlorophyll contents of the needles were significantly lower than 6.7-33.3% in the understory in the large，medium and small gaps (except the edge area)，and the lowest in each position of the large gap (5.8-33.1%)，showing a decreasing trend with gap size.However，the chlorophyll a/b ratio was significantly higher than that in the understory (8.6%) only in the transition area of the large gap.

Changes in the photosynthetic parameters of needles in different positions in the gap

Position in the gap (central，transition，edge) affected the photosynthetic parameters of pine needles differently(Fig.2).Values ofPmaxin the central area of the large，medium and small gaps were significantly higher than those in the transitional and edge areas by 20.3-21.5% and 47.1-66.2%，respectively，and in the transition area they were significantly higher (P＜0.05) than those in the edge area by 22.1-38.1% (Fig.2 A).Therefore，Pmaxdecreased from the centre to the transition and to the edge area in gaps of different sizes.

The LSP was significantly higher than in the edge area in the central and transition areas in the large gap，but there was no significant difference between positions in the middle and small gaps (Fig.2 B).LCP increased regularly in the central area，and the transition to the edge area in the large and medium gaps，but values for the central area and the transition area in the small gap were significantly lower than for edge area (Fig.2 C).The influence of the gap position on AQY was consistent with its influence onPmax，as it decreased along the centre，and the transition to the edge in the large and medium gaps.In the small gap，the values in the central and transition zones were significantly higher than those in the edge area (Fig.2 D).Transpiration rates(Tr) in the central area of the large and small gaps were significantly higher than those in the edge area，and there was no significant difference between positions in the medium gap (Fig.2 E).Stomatal conductance (Gs) of needles in the central area of the large gap was significantly higher than in the edge area，and in the central and transition areas in the small gap，Gswas significantly higher than in the edge area(Fig.2 F).Intracellular CO2concentrations (Ci) were only significantly higher in the central area of the small gap but there was no significant difference between positions in the large and medium gaps (F i g.2 I).Similarly，WUE and Rddid not show significant differences among different position in gaps (P＞ 0.05;Fig.2 G，H).

Therefore，in the large and medium gaps，LCP increased along the centre，and the transition to the edge area，but AQY decreased，while in the small gap，LCP was lower in the centre and the transition area than in the edge area.AQY was higher in the central and the transition areas than in the edge area.In addition，LSP in the large gap was higher in the central and the transition areas than in the edge area，and Tr and Gswere higher in the central area than in the edge area.

Different tree positions in the gap had a significant effect on chlorophyll a，chlorophyll b and total chlorophyll levelsbut had no effect on the chlorophyll a/b ratio (Fig.3).Chlorophyll a and total chlorophyll showed an increasing trend in the large，medium and small gaps along the central area and the transition to edge area.Chlorophyll b also increased trend in the large and middle gaps along the central and the transition areas relative to the edge area，but in the small forest gap，values in the central and transition areas were significantly lower than those in the edge area.

Fig.3 Chlorophyll content and ratio of chlorophyll a to b of needles of Korean pine in different gap sizes.Notes Chl a:chlorophyll a (A);Chl b:chlorophyll b (B);Chl T:total chlorophyll (C);Chl a/b:ratio of chlorophyll a to b (D).CA:central area;TA:transition area;EA:edge area.Different lowercase letters indicate significant differences between gaps of different sizes，and different capital letters indicate significant differences between positions (P＜0.05)

Impact factors of the maximum net photosynthetic rate

Pmaxand other photosynthetic parameters and environmental factors were obtained by multiple stepwise regression analysis;thePmaxwas mainly affected by AQY in the large gap and AQY explained 29% ofPmax(Table 2).In the medium forest gap and forest understory，Pmaxis affected by light transmittance，explaining 31% and 24% ofPmax，respectively.In the small forest gap，it is mainly affected by LCP，accounting for 30% ofPmax; thePmaxwas mainly affected by LSP，AQY and total chlorophyll content in the centre of the gap，and the three variables explained 50.7% ofPmax.In the transition area，Pmaxwas mainly affected by LSP，explaining 23.5% ofPmax; in the edge area，Pmaxwas mainly affected by TL and Chl T.The TL and Chl T accounted for 22.8%ofPmax.

Table 2 Impact factors of the maximum net photosynthetic rate of Korean pine needles

There is a significant linear positive correlation betweenPmaxand AQY in the large gap (P＜0.001) (Fig.5).There was a highly significant or significant linear positive correlation with light transmittance in the middle gaps and forest understory，and a highly significant linear negative correlation with LCP in the small gaps (P＜0.001).Figure 4 shows that in the central area of the gap，there is a significant linear positive correlation betweenPmaxand LSP，AQY and total chlorophyll.In the transition area，Pmaxand LSP had a highly significant linear positive correlation (P＜0.001);in the edge area，Pmaxhad a significant linear positive correlation with TL (P＜0.01)，and a highly significant linear negative correlation with Chl T (P＜0.001).

Fig.5 Variation of the maximum net photosynthetic rate of Korean pine with impact factors in each gap.Notes Pmax:maximum net photosynthetic rate;LT:light transmittance (A);AQY:apparent quantum yield (B);LCP:light compensation point (C).LG:large gap;MG:medium gap;SG:small gap;U:understory.* P＜0.05;**P＜0.01;***P＜0.001

Discussion

Photosynthetic adaptability of Korean pine needles to different gap sizes

In this study，Pmaxof Korean pine needles increased with gap size at the central and transition areas (large gap ＞ middle gap ＞ small gap=understory)，but it had a different trend at edge areas of gaps (large gap=middle gap ＞ small gap=understory).This shows that the larger the gap，the higher thePmaxof the Korean pine needles，indicating that the young tree (35-year-old) stage in the gap in the temperate secondary forest have obvious light limitations.This is consistent with the findings that seedlings of numerous tree species in temperate deciduous forests and tropical rain forests，as well as 15-year-old saplings of Korean pine in the broad-leaved Korean pine forest of the Changbai Mountains，are light tolerant (Wang and Fan 2009;Riichi et al.2017;Santos and Ferreira 2020).However，Wang and Fan (2009) only measured the photosynthetic rate of 15-year-old Korean pine saplings during the vigorous growth period in July，and found that limiting the gap to 267-332 m2was more conducive to the growth of Korean pine，while in this study，the photosynthetic rate of 35-year-old Korean pine saplings was measured throughout the growing season (May to October)，and it was found that a gap of 200 m2was more conducive to Korean pine growth.At the same time，a suitable gap size is about 200 m2(the ratio of gap diameter to the surrounding highest tree height (d/h) is about 1.0)，which suggests that the best ratio of d/h for the growth of young shade-tolerant species or later succession species is similar to the finding that the regeneration and growth of seedlings should be＜1.00 (Malcolm et al.2001).This is obviously different from the large gap of 650-980 m2required for photosynthesis and growth of shade-intolerant seedlings ofQuercus mongolica(Zhang and Yi 2021).Due to differences in the characteristics of the tree species，the photosynthesis of intolerant species such asQuercus mongolicahas greater requirements for gap size than a shade-tolerant Korean pine.

Fig.4 Variation of the maximum net photosynthetic rate of Korean pine in each position with impact factors.Notes Pmax:maximum net photosynthetic rate;TL:temperature leaf (A);LSP:light saturation point (B);AQY:apparent quantum yield(C).Chl T:total chlorophyll D CA:central area;TA:transition area;EA:edge area.*P＜0.05;**P＜0.01;***P＜0.001

The larger the gap，the higher thePmaxof the needles;there may be several reasons for this.First，the size of the gap affects the amount of light entering the gap (Messier et al.1998)，thereby improving the regeneration and growth of species that have higher light and nutrient requirements(Sack et al.2006).On the other hand，photosynthesis is a complex process，which is not only affected by external environmental factors but is also influenced by the plant’s conditions (Calfapietra et al.2005).LSP，LCP and AQY of plants are important indicators of light utilization ability.Generally，plants with higher AQY and lower LCP have stronger shade tolerrance (Craine and Reich 2005)，and those with higher LSP and lower LCP have stronger ecological adaptability(Huang et al.2013).In this study，the light transmittance of the central and transitional areas of the gap increased with gap size (Table 1)，which in turn makes the LSP of needles in the central and transitional areas of the large and medium gaps increase with gap size.The variation tendency is the same asPmax(Fig.2A，B).However，LCP decreased as gap size increased (Fig.2 C)，making its AQY significantly higher than that in the understory (Fig.2 D).This is consistent with the high LSP and low LCP of Korean pine needles which can utilize both strong and weak light (Huo and Wang 2007).It is precisely because the needles of Korean pine have long adapted to the light environment in gaps of different sizes that the needles under strong light conditions show photosynthetic characteristics of sun-tolerant leaves (Zhao et al.2010)，thereby improving their adaptability in large gaps (LSP and AQY increased，while LCP decreased)，so thatPmaxincreased with gap size.

Secondly，the opening of the canopy increases the direct radiation and temperatures near the ground (Malcolm et al.2001).Average leaf temperatures increased the most in different positions in the large gap (1.5-1.9°C)，while the increase in medium and small gaps was smaller (0.2-1.1°C)(Table 1).The increase in air temperatures in the large gap significantly increased Tr and Gsof needles in the central and transitional areas (Fig.2 E，F(xiàn)).The increase in Gscan maximize the absorption of CO2，which helps increase the assimilation rate of photosynthetic carbon (Kirschbaum and Pearcy 1988;Sack et al.2006) and facilitates the exchange of water vapor with the air so that Tr and Pnare simultaneously enhanced (Guo et al.2006).In addition，the Rdof needles in different positions in the gap was，in general，significantly lower than that in the understory (Fig.2 H).This may be related to the suppression of dark respiration of plants under higher light conditions (Sun et al.2016).Rdvalues in the understory were higher than those in the gap.This means that Korean pine saplings need to consume more material and energy in the forest to adapt to low-light environments to complete their life cycle than they do in forest gaps.The low dark respiration rate in the gap ensures low consumption of photosynthetic products (Heimann and Reichstein 2008) and，at the same time，creates a higher photosynthetic efficiency (Pmax/Rd) conducive to the high growth of Korean pine in the gap.

Chlorophyll a，chlorophyll b and total chlorophyll levels in the needles in the large gap were significantly lower than those in the understory，and showed a decreasing with gap size (Fig.3).This indicates that needles of Korean pine absorb light energy by increasing the chlorophyll content under low light conditions in the understory，and adapt to the low light environment.This is consistent with the finding that chlorophyll content ofCastanopsis kawakamiiHayata seedlings in subtropical evergreen broad-leaved forest gaps is signif ciantly lower than in non-forest gaps (He et al.2019).

Photosynthetic adaptability of Korean pine needles to different gap positions

ThePmaxof Korean pine needles in various sized gaps decreased along the gradient from the central area，the transition area to the edge area，showing obvious photosynthetic adaptability.This is similar to the results of previous studies in whichPmaxvalues of one-year-old seedlings ofQ.mongolicawere the highest in the center of the large gap (Zhang et al.2018) or increased as the distance between the seedling and the center decreased in the large and medium gaps (Zhang and Yi 2021).This is similar to the finding that the Pnof 3-year-old Manchurian walnut (Juglans mandshuricaMaxim.) seedlings，a medium shade-tolerant species，reached its peak near the center of the gap (Lu et al.2021).The difference between these and our results is that the more shade-tolerant 35-year-old Korean pine also had the highestPmaxin the center of the gap.

ThePmaxof Korean pine needles in gaps of various sizes decreased along the microenvironmental gradient from the central area，the transition area to the edge area.The amount of light entering the gap depends not only on gap size but also the tree’s position within the gap (Messier et al.1998).The microenvironment (photosynthetically active radiation，air and soil temperature，humidity) between different locations in the gap have a large divergence (Luo et al.2020).The transmittance of photosynthetically active radiation in the central area of the gap is especially higher than in the edge area (Canham 1989;Brown 1996;Ritter 2005;Gálhidy et al.2006).Light transmittance in the large and medium gaps in this study decreased in the central area ＞ transition area ＞ edge area.Light transmittance in the small gap showed a central area=transition area ＞ edge area (Table 1).This occurs most probably because the needles of Korean pine have adapted to the light environment at different locations in the gap over time.Accordingly，the LCP of Korean pine needles in the large and medium gaps increased of central area＜transition area＜edge area.Values of AQY decreased of central area ＞ transition area ＞ edge area.In the small gap，the LCP showed a change of central area=transition area＜edge area，and the AQY a change of central area=transitional area ＞ edge area (Fig.2 C，D).This shows the values ofPmaxof Korean pine needles decreasing along the central area，transition area to edge area in different size gaps.

Additionally，the average temperatures in the growing season of Korean pine in the central area of the large，medium and small gaps were higher than those in the edge area(0.4-0.8°C) (Table 1).Tr and Gsin the central area of the large and small gaps were significantly higher than those in the edge area (Fig.2 E，F(xiàn)).This will inevitably cause changes in the gas exchange and transmission capacity between Korean pine needles and the atmosphere.The increase in stomatal conductance (Gs) can promote the absorption of CO2，thus increasing Pn(Kirschbaum and Pearcy 1988;Sack et al.2006) and is conducive to the exchange of water vapor with the atmosphere so that Tr and Pnare simultaneously enhanced-(Guo et al.2006).Therefore，Korean pine needles in the centre of the gap not only have relatively high light energy utilization but also have high gas exchange and transmission capabilities，which signif ciantly increases Pmax.

Chlorophyll a，chlorophyll b and total chlorophyll in needles in the edge area of gaps of different sizes were the highest，and increased along the gradient of the central area，transition area to edge area (Fig.2).This result is at odds with studies that gap position had no effect on total chlorophyll content ofQ.mongolica，J.mandshuricaandPicea koraiensis(Lu et al.2021).From the change in environmental factors in the gap at its initial stage of formation，it may be concluded that this has little effect on the photosynthesis of the emerging leaves of tree species with different degrees of shade tolerance (Zhang et al.2 018).While the gaps in this study were at a relatively mature stage of development，young Korean pine trees (35-yearsold) which are more shade-tolerant，have adapted to the light conditions at different locations in the gaps over time，which leads to differences in chlorophyll content.Chlorophyll levels of Korean pine were highest in the edge area of the gap where light is weakest，which helps to absorb more light energy to adapt to the low light environment and maintain photosynthetic capacity.

Conclusions

In this study，gap size and different positions of trees in the gaps in thePopulus davidianaforest had significant effects on the photosynthetic characteristics of 35-year-old Korean pine.ThePmaxincreased with gap size in the central and the transition areas in the gap.Along the microenvironmental gradient of the central，transition，to the edge areas of gaps of different sizes，Pmaxdecreased regularly.This indicates that the needles of young Korean pine have the strongest photosynthetic capacity in the central area of the large gap，and there is evident photosynthetic adaptability.At the same time，this species has two survival strategies:to grow rapidly in the gap under strong light conditions，and to maintain survival under the shade and low light conditions in the forest understory.Therefore，in afforestation management based on gaps，tree species can be planted according to gap size and position in the gap to improve space utilization.For example，in the central area of a secondary forest gap of about 200 m2(the ratio of the gap diameter/the highest tree height around ≈ 1.0)，Korean pine maybe planted in a cluster or surrounded by older planted Korean pine for liberation cutting，which is more conducive to the growth and regeneration of young Korean pine.

AcknowledgementsThe authors are very grateful to Dr.Yue Wang from the College of Life Science of NEFU for revising the manuscript to improve the paper.