The impact of the environmental factors on the photosynthetic activity of common pine(Pinus sylvestris)in spring and in autumn in the region of Eastern Siberia

N.E.Korotaeva•M.V.Ivanova•G.G.Suvorova•G.B.Borovskii

Abstract The taiga coniferous forests of the Siberian region are the main carbon sinks in the forest ecosystems.Quantitatively,the size of the carbon accumulation is determined by the photosynthetic productivity,which is strongly influenced by environmental factors.As a result,an assessment of the relationship between environmental factors and photosynthetic productivity makes it possible to calculate and even predict carbon sinks in coniferous forests at the regional level.However,at various stages of the vegetative period,the force of the connection between environmental conditions and the productivity of photosynthesis may change.In this research,correlations between the photosynthetic activity of Scots pine(Pinus sylvestris L.)with the environmental conditions were compared in spring and in autumn.In spring,close positive correlation of the maximum daily net photosynthesis was identified with only one environmental factor.For different years,correlations were for soil temperature(rs=0.655,p=0.00315)or available soil water supply(rs=0.892,p=0.0068).In autumn within different years,significant correlation was shown with two(temperature of air and soil;rs=0.789 and 0.896,p=0.00045 and 0.000006,respectively)and four factors:temperature of air(rs=0.749,p=0.00129)and soil(rs=0.84,p=0.00000),available soil water supply(rs=0.846,p=0.00013)and irradiance (rs=0.826,p=0.000001).Photosynthetic activity has a weaker connection with changes in environmental factors in the spring,as compared to autumn.This is explained by the multidirectional influence of environmental conditions on photosynthesis in this period and by the necessity of earlier photosynthesis onset,despite the unfavorable conditions.This data may be useful for predicting the flow of carbon in dependence on environmental factors in this region in spring and in autumn.

Keywords Pinus sylvestris L.·Eastern Siberia·Correlations·Photosynthetic productivity ·Seasonal changes in environment

Introduction

Change in the intensity of photosynthetic reactions is one of the main plant responses to environmental changes.Interest in the environmental aspects of photosynthesis of coniferous trees grew increasingly in the last few years(Zarter et al.2006;Gea-Izquierdo et al.2010;Galvagno et al.2013;Verhoeven 2013;Kolari et al.2014;Moyes et al.2015).The influence of environmental conditions on the intensity of photosynthesis has been driven by its connection with global climate change(Fréchette et al.2011;Pagter and Arora 2013;Rapacz et al.2014).

The impact of environmental factors on photosynthetic activity of evergreen conifers was previously studied either in areas with low temperatures and weak solar radiation(Ensminger et al.2004;Suni et al.2003),or in highlands with higher air temperature and strong insolation(Zarter et al.2006;Monson et al.2002,2005).Air temperature appears to be a good predictor for the timing of the commencement of photosynthesis at high latitudes(Suni et al.2003).In subalpine forests,air and soil temperature and water availability determine the time when spring reactivation of intrinsic photosynthetic capacity as well as carbon uptake occurs,although there may be considerable variation from year to year as to when this important event takes place.Hence,this impact cannot be unified for the entire boreal zone(Monson et al.2005).

The impact force of the external factors affecting photosynthesis of Pinus sylvestris L.(Scots pine)in spring and autumn in Eastern Siberia differs from the force of the external factors in other regions.For example,the climate of Eastern Siberia is characterized by lower annual temperature(-1 °C for the period 1980–2008);higher intensity of insolation,due to the geographic latitude and sea level(height above sea level is 428 m);lower annual precipitation(350–380 mm)(database of the All-Russian Research Institute of Hydrometeorological Information,http://meteo.ru/),and prevalence of evaporation over precipitation(Shwer and Formantchuk 1981).Clearly,the environment of Eastern Siberia poses extreme conditions for the inhabiting plants.In Eastern Siberia,low air and soil temperature become major limiting factors for Scots pine classed as xerophyte(Suvorova 2009).Despite this,Scots pine is a dominant species in this region because;the soil moisture level is the key factor for maximal values of photosynthetic activity in pine,even in the seasons with various conditions(Rysin and Savelyeva 2008;Suvorova et al.2007b).

Nevertheless,when in spring the photosynthesis resumes abnormally early for Eastern Siberia(in the first decade of April),its intensity is limited by low soil temperature(Suvorova et al.2004).Thus,optimal ranges of environmental factors—within which the highest values of photosynthetic activity are achieved—alter both during the years differing in heat—and moisture availability and throughout the vegetation period(Suvorova et al.2005).The period of influence of the environmental factor that limits photosynthesis remains the same in different years.In spring this period(from April 1 to June 15)begins with the first signs of visible photosynthesis and is characterized by instability of the process;the air and soil temperature is the dominant factor limiting photosynthesis in this period.Available soil water supply(ASWS)is the main factor limiting photosynthesis during the summer(from June 16 to August 31).Irradiation is the main factor limiting photosynthesis in the autumn(around September 1—the first decade of November)(Suvorova 2009).

Our understanding of the reproductive process of Scots pine under Eastern Siberia climate conditions is limited.Study of photosynthetic carbon transformation by forest ecosystems on a regional scale is important for understanding the mechanisms of self-regulation of carbon-sink function.Also,the formation of biomass and prediction of carbon sink formation will be made easier with the help of long-term databases of climatic conditions.

According to our data,the maximum of photosynthesis have a direct relationship with carbon accumulation.We have shown previously that photosynthesis maximum in pine has a positive line dependence from photosynthetic productivity(r2=0.8–0.9),regardless of the conditions of a given year of observations(Suvorova 2006,2009).This property can be used as a basis for calculating the daytime and seasonal productivity of coniferous forests by the indices of their maximum daily intensity of photosynthesis.Further,using mathematical models,it was shown that maximal rate of photosynthesis have a direct linear correlation with the maximum activity of Ribulose-1,5-bisphosphate carboxylase/oxygenase,or RuBisCO,the initial enzyme link in the chemical binding of carbon(model efficiency ME=0.73)(Suvorova et al.2017).

In this research,part of our long-term investigations of the influence of the environment on photosynthesis is described.It sums up,the results of our comparison study of the relations between external factors and the maximum of daily net photosynthesis in Scots pine in spring and autumn in Eastern Siberia.We also utilized parametric(r2,coefficient of determination)and non-parametric (rs,Spearman’s correlation coefficient)criteria of analysis of correlation dependence.

Materials and methods

Plant material and study site

The experimental planting is located on the outskirts of Irkutsk(52°14′21′N,104°16′7′E).Geographically,this territory is a part of the Middle-Siberian plateau;an elevated plain dominated by gently sloping hills.The climate of the region is largely formed by the Siberian anticyclone.According to the Köppen climate classification,the climate of the southern part of Eastern Siberia is classified as Dwc:cool continental climate/subarctic climate(Peel et al.2007).Through most of the year,the weather in this region is dominated by continental air masses.Normally,in summer season when the air becomes warmer,the conditions favoring rainfall are formed and humid precipitation-bearing winds from the Atlantic penetrate the area(Kartushin 1969).

In general,the quantity of summer rainfall dominates the annual precipitation.In Irkutsk,the average air temperature amounts to-1°C;the average annual precipitation—359 mm;and the length of the growing season—130 days(Vaschuk and Shvidenko 2006).The territory is mainly characterized by widespread Scots pine forests,with inclusions of Siberian larch,spruce, fir,Siberian pine,birch,and aspen.The area studied is 80%forested,with coniferous species accounting for more than half of the forested area(Vaschuk and Shvidenko 2006).The experimental plantation was established in 1985 on the research field of the Siberian Institute of Plant Physiology and Biochemistry SB RAS with two-year-old seedlings,grown from local coniferous seeds supplied by a state-owned arboretum located in the settlement of Meget,Irkutsk District,150 km away from the study plot.

We used three Scots pine trees(Pinus sylvestris L.)(25 years old)grown at the experimental site of the institute.The stand is located on a gradual slope(2–3°)of eastern exposure.The plantation is characterized as follows:the species composition was 40%pine,30%spruce,and 30%larch;the crown density was 0.5–0.6,the average height of pine was 4.45 m;and the average stem diameter at the height of 1.5 m,was 68.8 mm.For the measurement of photosynthesis,three trees with characteristics of photosynthesis close to each other were selected.The soil is gray forest non-podzolized loamy,on Jurassic carbonaceous loams underlain by sand.Ground waters are located at a considerable depth(11–50 m)and do not produce a significant impact on the soil moisture mode.The investigation was conducted in 2007 and 2008.

Registration of the environmental factors

We monitored air and soil temperature,solar radiation(irradiance),soil moisture and precipitation abundance during the vegetation period every day at 1-hour intervals,as described previously(Suvorova et al.2007a;Korotaeva et al.2012).The ambient air temperature,the temperature in one of the assimilation chambers,and also the soil temperature at depths down to 120 cm were detected continuously on the measurement days with copper thermocouples,and the parameters were simultaneously recorded by a multi-point register KSM-4(GK Prompribor,Russia).

The relative air humidity in the middle part of the crown was measured with a hygrograph M-21 AN(Pilot factory of hydrometeorological devices,Russia),and the parameters were verified using Assman’s aspiration psychrometer(GK Prompribor,Russia).Soil moisture contents were determined for each 10 cm soil layer to a 100 cm depth every 10 days during the growth period using the thermostat-gravimetric method.ASWS was calculated by a commonly used technique(Fedorovsky 1975)as the difference between the soil moisture content and the moisture inaccessible for plants.The air humidity was determined on a weekly basis by a hygrograph and its readings were verified on a daily basis using an aspiration psychrometer.Solar radiation incident upon the tree canopy was measured with a pyranometer M-80(Hydrometpribor,Russia),connected with a potentiometer KSP-4(GK Prompribor,Russia)for automatic records.When converted pyranometer readings in energy units(W m-2)by the number of photons(μmol(photon)m-2s-1)the coefficient of 4.5 was used(Long and Hallgren 1989).

Registration of the net photosynthesis activity

Measurements of net photosynthesis activity were started when the first signs of positive gas-exchange were detected in early spring(in the middle of April)and finished when the process ended in the last ten days of October.The share of PAR(photosynthetically active radiation),which was determined according to Tooming(1977),during the growing season in clear weather was 48–52%.Net photosynthesis activity was monitored around the clock for three days of each week.Nine assimilation chambers,each reinforced with a wire frame and covered with polyethylene,were installed on the southern side of the middle part of the crowns of the trees studied,on the brachyblasts of the second year.

The volumes of the assimilation chambers were adapted to shoot sizes and were equal to 0.5 dm3.Free polyethylene ends of the assimilation chambers were fixed on branches with scotch tape.In addition,three CO2concentration measurements were taken in the ambient air near the chambers,for control.The CO2gas exchange of shoots was measured by an infrared gas analyzer Infralyt 4(Veb Combinat Mess-und Regelungstechnik,Germany)—based multi-channel device of open type.The values of the CO2content were fixed by the EPP-09 recorder(GK Prompribor,Russia).Registration of the content of CO2in gas analyzer was carried out with the help of a magnetoelectric galvanometer.Air flow was pumped by the compressors positioned between channel switches and the air dryer.The air entered the assimilation chamber via an air inlet;from there,it flowed around the needles,going to the CO2measuring device for analysis;and then coming out with the exhaust.The effectiveness of the device was checked by special methodical examination(Sherbatyuik et al.1991).

The rate of CO2absorption(mkmol m-2s-1)(net photosynthesis)was taken as the intensity of photosynthesis.To calculate it,the difference in the concentration of carbon dioxide in the control chamber and in the assimilation chamber was determined.To calculate the photosynthesis rate per unit of surface area of the needles,Tselniker’s tables were used(Tselniker 1982).The average values for the photosynthesis rate for each hour of the day for three trees were used to calculate the daytime(daily)average photosynthetic productivity(PSP).Measurements of the CO2content were carried out only in the daytime.The monthly value of PSP was estimated as a product of the average daily photosynthetic productivity by the number of days in the month.The daily photosynthetic activity maxima were selected according to the hourly parameters of the processes during each day.All values of the daytime assimilation maximum,which reached more than 80%of the maximum seasonal values(absolute seasonal maximum),were included in the range of the maximum values of photosynthesis.

Statistical analysis

The Shapiro–Wilk test was used to con firm the normality of variations.Standard linear regressions,coefficient of determination(r2),and Spearman’s correlation(rs)were used to assess the direction and level of the relation between the level of maximum daily net photosynthesis and environmental factors(Glantz 1999).During the correlation evaluation—between several pairs of characteristics—some lacked normal distribution;in response,the intensity of the correlation connection was assessed with Spearman’s non-parametric criterion(rs).

The statistical significance of the correlation was evaluated,using the table of critical values of Spirman’s range correlation ratio (p＜0.05)(Glantz 1999).Statistical analysis including determination of statistical significance of differences in Spearman’s correlation(p＜0.05)and analysis of the regressions were both performed by Statistica soft.The regression analysis included detection of the adequacy of the model to describe dependence(p＜0.05)and analysis of the prognostic significance of independent factor of environment(p＜0.05).Since the normality condition for the distribution of the quantitative variation series in some of the compared groups is not met,the multifactor ANOVA was not applicable.

Results

Peculiarities of vegetation periods 2007–2008

Fig.1 Hydrothermal conditions and solar radiation during the vegetation periods 2007 and 2008.1882–2008 years data(database of the All-Russian Research Institute of Hydrometeorological Information)were taken for the long-term average(Lta)of precipitation and monthly air-temperature means.Monthly soil temperature mean was determined at the depth of 5 cm.Data from the years 1998–2008 years(own research)were taken for Lta of monthly soil temperature mean.The data from 1880 to1980(Shwer and Formantchuk 1981)were taken for the Lta of monthly total solar radiation mean.We used our own data for the years 2002–2012 to determine the Lta of monthly available soil water supply mean.Abbreviations denote:Apr—April;Aug—August;Sept—September;Oct—October

The vegetation periods in 2007 and 2008 did not significantly differ in air temperature(except April),and were warmer than the average values over many years(Fig.1).The monthly soil temperature mean was higher than average values of many years in the first part of the vegetation season in 2007.This year was characterized by a high intensity solar radiation,which exceeded the average multi-annual monthly values from June to September.In contrast,the solar radiation level in the 2008 vegetation period in spring and in autumn was below the average multi-annual values and values in 2007.In early spring 2008,the ASWS was considerably lower than the previous years’indices and was attaining a peak low value over the previous year.

Photosynthetic productivity(PSP)

According to our data,over the observation period,the photosynthetic productivity in each of the months was higher in 2007(Fig.2).During the 2007 growing season,PSP had reached its maximum value in May.In 2008,PSP had the highest values in the period from May to September.

The impact of the external factors on maximal daily photosynthesis rate

In the periods between July–August 2007 and 2008,no significant impact of the environmental factors on photosynthetic activity was revealed.The maximal daily photosynthesis rate significantly depended on the environmental factors in autumn and spring.Analysis of the regressions demonstrated that derived regression models adequately described the dependence of the maximum daily photosynthesis rate on the environmental factors;all the environmental factors were significant at p＜0.05,except ASWS at 2008 autumn to a small degree(Table 1).In almost all of the cases,the relation of the maximal daily photosynthesis rate on environmental factors proved positive,except the dependence on ASWS in spring 2007(Fig.3c)and autumn 2008(Fig.3h).Differences in the Spearman correlation coefficients between any of the environmental factors were significant if one of the rshad a negative value(for example,ASWS in spring 2007,rs=-0.806).

Fig.2 The dynamic of the monthly photosynthetic productivity(PSP)of pine during vegetation periods of two years.The monthly PSP value was estimated as a product of the average daily photosynthetic productivity by the number of days in the month

In the fall of 2007 and 2008,the dependence of the photosynthetic activity on the environmental factors was statistically significant in all the cases except dependence on solar radiation in 2008.In spring 2007(Fig.3a–c)and in spring 2008(Fig.3h)dependence on environmental factors proved statistically significant in all cases:ASWS(rs=-0.806,p=0.004),the air(rs=0.72,p=0.0185)and the soil temperature(rs=0.655,p=0.003)in 2007 and on ASWS(rs=0.892,p=0.006)in 2008.

In spring 2007,as compared to spring 2008,photosynthetic activity was closely connected with a larger number of external factors(Fig.3).There was one exception:the intensity of solar radiation.In spring 2008,the dependence was statistically significant only with ASWS(rs=0.892,p=0.006)(Fig.3h).

In spring 2007 connection of photosynthetic activity with temperature of a soil(r2=0.683,p=0.003)and ASWS(r2=0.64,p=0.004)was a little closer than connection with the air temperature (r2=0.512,p=0.018)(Fig.3a–c,Table 2)However the difference turned up statistically inessential judging by Spearman’s correlation coefficients(Table 2).

Discussion

Conditions during the vegetation periods of 2007 and 2008 were characterized by some differences that apparently had an impact and changed photosynthetic activity of needles.The 2007 vegetation period may be characterized as more favorable than 2008,abnormally warm and productive.The 2008 vegetation period is characterized as warm,favorable from the viewpoint of humidity except during the spring.

Although a higher humidity was detected in the second part of 2008(Fig.1),PSP was higher in 2007 both in the first,and in the second part of vegetation season(Fig.2).Evidently,the primary distinguishing factor of 2007—a high level of solar radiation—allowed the trees to use environmental resources for photosynthesis to the maximum.In spring 2007 the high PSP level was correlated with higher temperature values and optimal ASWS,which in this period is the most important factor for photosynthesis onset(Monson et al.2005).

The negative correlation between photosynthetic activity and ASWS in this period is obviously accounted for by the fact that,due to an air temperature increase exceeding average multi-annual values,and low precipitation level inthis period(Fig.1),photosynthetic activity growth occurs simultaneously with intensive moisture evaporation from the soil surface and reduction of its humidity.In June 2007,the solar radiation level was high and evidently favored PSP along with optimal soil moisture level(Figs.1,2).In September 2007,the rise of soil moisture level produced a belated effect,as a large amount of precipitation fell in July,with optimal soil and air temperatures persisting in September.As a result,the physiologically important upper 50-cm soil level could cool more slowly,which also favorably affected PSP.

In 2008, fluctuations in PSP were smoother and corresponded to seasonal changes in environmental conditions.A reduction in ASWS in autumn 2007 and in temperatures of soil(or air)in April 2008,compared with 2007,affected PSP in 2008:it turned out to be low as in 2007(Figs.1,2).Lack of correlation between photosynthetic activity and environmental conditions in summer apparently is related to the fact that,in the warm period of the year,the photosynthetic activity of mesophyll tends to fully realize the photosynthetic potential,provided it is not limited by environmental factors including water availability and the absence of summer droughts(Suvorova 2009).

In spring 2008,unlike the spring of 2007,no correlation of the maximum of daily net photosynthesis rate with environmental conditions was observed,apart from a significant correlation with ASWS changes(rs=0.892,p=0.0068)(Fig.3h).Apparently,during this time PSP was considerably suppressed due to the preceding drought(Fig.1).The absence of statistically significant correlation connections with other environmental factors in spring 2008 presumably is accounted for by the fact,that given the extreme value of one of environmental factors,the impact of other factors becomes less significant.The negative connection between photosynthetic activity and ASWS in autumn 2008(Fig.3i)may be explained by the high precipitation level and relevant ASWS growth(Fig.1)The second explanation is an autumn decrease in photosynthetic activity with the reduction of solar radiation level,as a direct limiting effect of excessive moisture on photosynthesis.

In spring,photosynthesis depends on the air temperature.The influence of the temperature may be conditioned by a simultaneous reduction in mesophyll conductivity and in enzyme activity(Bauer et al.1994;Dahal et al.2012),or by partial destruction of green pigments(Suvorova et al.2011)or by photoinhibition(Hansen et al.1996;Vogg et al.1998).The presented data demonstrate that photosynthesis in spring is closely connected with soil status that con firms the findings of previous studies(Suvorova et al.2004,2005,2007a,b;Ensminger et al.2008).Even with the increase of air temperature up to the optimal values,the cooling of pine roots takes place,which results in low hormonal and trophic status of roots,limiting the achievement of high PSP values(Ensminger et al.2008;Suvorova 2009).

The equations given in the article do not fully re flect the dependence of the maximum of daily net photosynthesis on ASWS in autumn 2008(Table 1).A sharp decline in maximal daily photosynthetic activity during this period(Fig.3i),which is explained by an hasty transition to negative air temperatures in the middle of the measurement period,apparently,was the reason of this discrepancy.

According to our data,in spring 2007 differences in the force of the correlation of the maximal daily photosynthesis rate with air and soil temperature were insignificant,despite the fact that the correlation with the soil temperature has higher level of correlation coefficient and smaller value of p in comparison with the air temperature(r2=0.683,p=0.00024 and r2=0.512,p=0.0198,respectively for soil temperature and for air temperature)(Fig.3a,b,Table 2).Our findings show that during spring in Eastern Siberia,photosynthetic activity apparently is determined by the temperature of air and soil conditions(its humidity and temperature)in the equal extent.Thus,the conditions of the beginning of growth in Eastern Siberia are closer to the conditions of subalpine zone described by Monson with co-authors(2005).

As we see,in spring 2007 and 2008,attainment of the maximal daily photosynthesis rate has a direct and close relationship with fewer environmental factors,as compared to autumn(Fig.3).Such peculiarity is observed both in 2007 favorable for PSP,and less favorable in 2008.Perhaps this is accounted for by the fact,that in spring,unlike autumn,the impact of the environmental factors has a multidirectional character.For example,in spring of 2007 and 2008,a sufficiently high level of intensity of sunlight begins to act on pine needles much earlier than the optimum of the temperatures of air and soil for the onset of photosynthesis appears;on the contrary,in autumn all investigated environmental factors affect photosynthesis simultaneously(Fig.1).

In spring,photosynthetic activity is oppressed by cooling of the root system,which reduces the degree of influence of other factors(Schwarz et al.1997;Ensminger et al.2008).In late spring,cooling of the roots ceases and growth processes are renewed(Repo et al.2005).During this period,the growth of pine mainly occurs due to the recently produced metabolites after activation of photosynthesis(Hansen and Beck 1994).Therefore,photosynthesis in spring is activated in response to a powerful request for photosassimilates,despite unfavorable conditions.In spring,the influence of the environmental factors on photosynthesis has a controversial character,which results in the necessity to activate it in unfavorable environmental conditions and requires the presence of protective factors,which,as a rule,are necessary during the cold season(Korotaeva et al.2012,2015).

Conclusions

Although both years of observation were favorable for the photosynthesis,one of the years contributed to a particularly complete realization of the photosynthetic potential of pine.This was reflected in the increased productivity of photosynthesis in a more favorable year.Despite the differences in conditions and photosynthetic activity in different years,the force of the correlation between photosynthetic productivity and environmental conditions was higher in the autumn than in the spring.In spring,differences in the force of the correlation of the maximal daily photosynthesis rate with air and soil temperature were insignificant.Our research shows that in Eastern Siberia implementation of the maximums of photosynthetic activity in spring depends on environment weaker than in autumn,which makes using of multi-year databases unsuitable for prediction of carbon sinks in spring,especially in years with less favorable environmental conditions,when correlation is very slight.As far as we know,this is the first such study in the Eastern Siberia region.

AcknowledgementsThe authors express their gratitude to L.D.Kopytova and L.S.Yan’kova for their contribution to the acquisition of the experimental data on ASWS and PSP.