Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil
chemical properties in the long-term provenance experiment in the Western Sayans
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Biomass and activity of soil microorganisms under
different pine species and climatypes
Naumova N.*, Makarikova R.*, Kuznetsova G.**
* Institute of Soil Science and Agrochemistry SB RAS
** Sukachev’s Institute of Forest SB RAS
Abstract
In the long-term field provenance experiment in the south of Krasnoyarsk region (Russia)
the influence of inter- and intraspecies heterogeneity of pines (Pinus sibirica Du Tour and Pinus
koraiensis Sieboldd et Zucc.) on some soil microbiological properties (soil microbial biomass C
and N, their ratio to soil organic C and N, soil basal and substrate-induced respiration,
metabolic and respiratory quotients) was studied. Under Siberian pine as compared to the
Korean one, the bulk soil showed higher substrate-induced respiration (13.4 vs. 11.5 μl • hr-1 • g1
soil), while the rhizosphere soil had increased microbial biomass C (590 vs. 413 μg С • g-1 soil)
and its contribution into soil organic matter (1.1 vs. 0.9 %). Interspecies heterogeneity of pines
displayed different patterns of its effect on soil microbiological properties: the effect of Siberian
pine climatypes was found to be statistically significant in multivariate and univariate (microbial
N content, 11 - 15 μg • g-1 soil) ANOVA, while the effect of Korean pine climatypes was found to
be statistically significant only in univariate ANOVA as concerned soil basal respiration (1.9 vs.
2.3 μl • hr-1 • g-1 soil) and its ratio to substrate-induced respiration (0.17 vs. 0.19).
The interspecies differentiation of the studied pines in their growth and development
properties (tree height and its annual increment, crone and trunk diameters, as well as
branching pattern) was shown to correlate mainly with microbial biomass C/N ratio and
substrate-induced respiration, while their intraspecies differences were positively correlated
with soil basal respiration and respiratory quotient, i.e. the ratio of active to potentially active
microorganisms, while being negatively correlated with microbial N and its contribution into
soil organic N.
Overall the variability of soil microbiological properties to a greater extent was
determined by the immediate influence of pine roots, i.e. rhizosphere effect, than by inter- or
intraspecies variability of physiology, biochemistry and productivity of the studied pines. Thus
studying the structure and development of woody plants’ root systems should be getting more
attention both in soil ecological studies and in planning tree use for technological purposes.
Keywords: PINUS SIBIRICA DU TOUR, PINUS KORAIENSIS SIEBOLDD ET
ZUCC., CLIMATYPE, GREY SOIL, RHIZOSPHERE, SOIL MICROBIAL BIOMASS, SOIL
RESPIRATORY ACTIVITY, LONG-TERM PROVENANCE EXPERIMENT, THE
WESTERN SAYANES
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Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil
chemical properties in the long-term provenance experiment in the Western Sayans
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Introduction
Increasing use of coniferous tress for reclamation of disturbed territories [1], growing
protective forest belts [2], parks and forest culture [3, 4], as well as changes in forest woody
plants composition due to global warming [5, 6, 7, 8 ], all together significantly enhanced both
the importance of the choice of tree species for the intended use and actuality of “plant-soil”
interaction studies to acquire a more detailed insight of the effect of various plant species,
climatypes and cultivars exert on soil properties.
Plant material input on/into soil is the main carbon and energy source for most soil
microorganisms. The quantity and quality of plant material with above- and below-ground litter
and exudates depends on the inter- and intraspecific variability of productivity, physiology and
biochemistry of the main forest-forming tree species [9, 10] and their changes due to the
influences of various factors, such as pathogens, recreation, etc.
The roots of trees are well developed, reaching deep into the soil and subsoil and hence
influencing large soil amounts. Therefore the rhizosphere is an important interface of tree-soil
interaction, root exudates being the major source of available carbon substrates for soil
microorganisms [11]. Changes in chemical composition and/or amount of root exudates can
significantly affect soil microbial community activity and composition [12, 13].
In practice it is quite difficult to differentiate between the influence of soil properties on
plant growth and development and, vice versa, the influence of plants on soil properties.
However, in Russia there are long-term field provenance experiments with various tree species
and their climatypes [14, 15] set up in 1960-70s. These experiments represent unique objects,
providing, among others, the possibility to investigate the influence of trees on soil microbial
properties.
The aim of this work was to study the influence of genotypic heterogeneity of pines on soil
microbial biomass and activity, in particular, in the rhizosphere, in the long-term (over 30 years)
field provenance experiment.
Materials and methods
The provenance experiment with different pine species and their climatypes was set up in
the Ermakovo Forestry of the Krasnoyarsk region, Russia, in 1983. The experiment is described
in details elsewhere [16]; briefly, 10,000 seedlings of Siberian pine (Pinus sibirica Du Tour) and
Korean pine (Pinus koraiensis Sieboldd et Zucc.) were planted on 1 hectare with 1.5 m between
Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil
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rows and 0.7 m between individual plants. The Siberian pine was represented by 3 climatypes,
namely, from Tashtagol (Kemerovo region, Russia), Shegar (Tomsk region, Russia) and
Ermakovo (Krasnoyarsk region, Russia), i.e. the climatype that grows in the immediate vicinity
of the field experiment plot and by default better adapted to the environment. Prior to experiment
start the soil was cleared and ploughed, and hence is anthropogenically transformed grey soil.
The experiment was set up and has been maintained since in triplicate plots, so each climatype
occupies one subplot on each experimental plot.
Soil was collected in August 2013 from 0-20 cm layer (immediately below the litter layer
and with maximal root density) 60 cm from the tree row within the crone zone [17]. One
composite sample was mixed from 6 individual soil monoliths. Rhizosphere soil was collected as
the soil remaining on 1-3 cm pine roots after their gentle shaking [18].
Soil chemical properties in the experiment were described earlier [19].
Soil microbial biomass carbon (SMBC) and nitrogen (SMBN) contents were estimated by
fumigation-extraction methods [20, 21]. Briefly, moist soil was fumigated with ethanol-free
chloroform for 24 hours in the dark at 25 оС. Then aliquots of the control (non-fumigated) and
fumigated soil were extracted with 0.5 M K2SO4 solution (1: 4 w/v), and suspensions filtered
through ammonium-free filters. The obtained extracts were analyzed for total nitrogen and
organic carbon content by Kjeldahl and dichromate oxidation methods, respectively. Then
SMBC was calculated as the difference in organic C content in extracts from fumigated and
control soil, divided by 0.35 [21], and SMBN content was calculated as the difference in total
nitrogen content in extracts from fumigated and control soil, divided by 0.54 [20]. Then by
dividing soil microbial biomass C and N by soil organic carbon (SOC) and nitrogen (SON)
content we estimated their respective contribution into soil organic matter.
Soil basal respiration (CO2) was estimated by measuring CO2 evolved by soil after
stabilization and without any amendments [22]. Substrate-induced respiration (SIR) was
estimated by measuring CO2 evolved by soil after glucose addition at the rate of 0.8 mg С∙ g-1
o.d. soil to stimulate mainly bacterial growth [23]. The respiratory quotient (QR) was calculated
as a ratio of the basal to the substrate-induced respiration [24], while biomass metabolic quotient
was calculated as a ratio of basal respiration to microbial biomass carbon [25].
Statistical analysis (PCA and ANOVA) of the log-transformed soil microbiological data
was performed by using Statistica v.6.1 software package.
Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil
chemical properties in the long-term provenance experiment in the Western Sayans
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Results and discussion
Effect of interspecies heterogeneity of pines
The obtained estimates of soil microbiological properties (Tab. 1) in general coincide
with the data published earlier for topsoils (without litter) of coniferous forest ecosystems [26,
27, 28, 29]; however, there are few estimates for rhizosphere of coniferous trees. ANOVA
revealed neither statistically, nor ecologically (the contribution into the total data variance less
than 5%) significant effect of pine species on almost all the studied soil microbiological
properties, except for substrate-induced respiration (Tab. 2). This parameter was higher in soil
under Siberian pine (Tab. 1), most likely resulting from the more pronounced physiological
reaction of microorganisms, actively growing or capable to begin growth immediately or several
hours after addition of easily available carbon substrates [30], i.e. active and potentially active
microorganisms [24].
The effect of soil (the bulk vs. rhizosphere soil) on the variability of soil microbiological
properties was much more pronounced as compared to the effect of pine species (Tab. 2), as it
was revealed in most of the studied properties, accounting for significant part of their total
variance. For example, SMBN and its ratio to SON, as well as basal respiration and QR in the
rhizosphere of both pine species, were found to be twice as high as in the bulk soil (Tab. 1). The
findings confirm the relatively higher content of active microorganisms in the rhizosphere [30]
due to more comfortable environment there because of the availability of carbon and energy
substrates [24]. Soil microbial biomass C/N ratio in the rhizosphere was found to be quite
decreased, most likely due to the difference in physiological status of rhizosphere
microorganisms, as actively growing cells are enriched in nitrogen compounds. It was reasonable
to assume that interspecies tree differences can be more explicit in the rhizosphere. Indeed,
ANOVA of the rhizosphere soil data only showed the effect of pine species on SMBC (P =
0.056) and its ratio to SOC (P = 0.072), the respective values being 1.4 and 1.2 times higher
under Siberian pine (Tab. 1), confirming increased availability of organic substrates in the
rhizosphere of the species [31] and increased microbial biomass contribution into humus
formation [32].
Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil chemical properties in the long-term provenance
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Table 1. Soil microbiological properties under different pine species (mean ± s.e.m.)
Pine
Siberian pine
Parameter
Korean pine
Bulk soil
Rhizosphere soil
Bulk soil
Rhizosphere soil
SMBC, μg С • g-1 o.d. soil
445 ± 84
590 ± 89
561 ± 70
413 ± 76
SMBN, μg N • g-1 o.d. soil
13 ± 1,5
29 ± 8
11 ± 1,3
23 ± 7
SMB С/N
44 ± 8,5
30 ± 11
66 ± 9,2
22 ± 2
CO2, μl • hr-1 • g-1 o.d. soil
2.4 ± 0.2
4.5 ± 0.1
2.1 ± 0.2
4.2 ± 1.7
SIR, μl • hr-1 • g-1 o.d. soil
13.4 ± 0.4
13.9 ± 1.4
11.5 ± 0.7
10.3 ± 0.9
QR
0.18 ± 0.01
0.33 ± 0.03
0.18 ± 0.02
0.40 ± 0.13
Qmet, μg С-СО2 • mg SMBC-1 • hr-1
3.7 ± 0.8
3.8 ± 0.1
2.0 ± 0.3
4.8 ± 1.2
SMBC/SOC, %
1.4 ± 0.3
1.1± 0.1
1.7 ± 0.1
0.9 ± 0.0
SMBN/SON, %
1.1 ± 0.1
2.2 ± 0.6
1.0 ± 0.1
2.4 ± 0.5
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Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil
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Table 2. Results of the univariate and multivariate ANOVA for soil microbiological properties
under different pines: factor contribution into the total variance (%) and
significance level
Factor
Variate
Pine species
Soil
Interaction
(A)
(B)
(А x B)
SMBС
2 (0.78)
1 (0.99)
10 (0.19)
SMBN
4 (0.28)
47 (0.00)
1 (0.62)
SMB С/N
2 (0.59)
6 (0.23)
24 (0.03)
CO2
2 (0.47)
1 (0.96)
59 (0.00)
SIR
1 (0.68)
3 (0.37)
38 (0.01)
QR
2 (0.32)
2 (0.39)
66 (0.00)
Qmet
1 (0.72)
11 (0.14)
9 (0.18)
SMBC/SOC
1 (0.81)
14 (0.11)
3 (0.42)
SMBN/SON
1 (0.87)
2 (0.52)
53 (0.00)
All variates
(0.14)
(0.07)
(0.03)
Note: values P ≤ 0.05 are shown in bold.
Effect of intraspecies heterogeneity of pines
The obtained estimates of microbiological properties of the bulk soil, sampled from under
different climatypes of both pine species, did not vary much due to the intraspecies variability of
pines (Tab. 3). Nevertheless, the performed multivariate ANOVA revealed statistically
significant effect of climatypes in soil under Siberian pine and no effect under Korean pine
(Tabs. 4, 5). As for the univariate ANOVA results, under Siberian pine the effect of climatype
accounted for about 1/3 of the variance of SMBN and of its ratio to total soil nitrogen, as well as
SIR (Tab. 4). Under Korean pine the effect of climatype was found for soil basal respiration,
accounting for almost half of its variance (Tab. 5) and for QR (Tabs. 4, 5), accounting for about
1/3 of its variance. Basal respiration was estimated to be 1.6 times more intensive under
Khabarovsk climatype of the Korean pine as compared to the Primorsk one, in other words the
difference between climatypes concerning soil microbial metabolic activity can ecologically be
quite significant and lead to different intensity of organic matter mineralization in soil under the
trees.
For some soil properties such as SMBN and of its ratio to total soil nitrogen, as well as
Qmet, in soil under Korean pine ANOVA showed the significance level of the climatype effect
ranging 0.05 ≤ P ≤ 0.10 (Tab. 5), which can also be regarded as statistically significant, if we
raise significance level to P ≤ 0.10, as it is sometimes proposed for ecological studies [33]. Yet
the multivariate ANOVA did not reveal the effect of climatype for Korean pine, which may be
explained by the less number of climatypes of the species in the experiment.
Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil chemical properties in the long-term provenance
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Table 3. Some microbiological properties of the bulk soil under different climatypes of the two pine species (mean ± s.e.m.)
Parameter
Siberian pine
Korean pine
climatypes
climatypes
Kemerovo
Ermakovo
Tomsk
Khabarovsk
Primorsk
SMBC, μg С • g-1 o.d. soil
551 ± 207
491 ± 120
322 ± 203
577 ± 127
544 ± 92
SMBN, μg N • g-1 o.d. soil
11 ± 3
12 ± 2
15 ± 2
10 ± 2
11 ± 1
SMB С/N
61 ± 19
47 ± 10
24 ± 7
70 ± 13
62 ± 15
CO2, μl • hr-1 • g-1 o.d. soil
2.2 ± 0.4
2.9 ± 0.5
2.0 ± 0.1
2.3 ± 0.2
1.9 ± 0.3
SIR, μl • hr-1 • g-1 o.d. soil
13 ± 0.8
13 ± 0.8
14 ± 0.7
12 ± 0.8
11 ± 1.1
0.17 ± 0.03
0.21 ± 0.04
0.16 ± 0.01
0.19 ± 0.03
0.17 ± 0.02
Qmet, μg С-СО2 • mg SMBC-1 • hr-1
2.7 ± 0.9
4.0 ± 1.9
4.3 ± 1.8
2.2 ± 0.6
1.7 ± 0.2
SMBC/SOC, %
1.7 ± 0.7
1.5 ± 0.5
0.9 ± 0.3
1.7 ± 0.2
1.8 ± 0.2
SMBN/SON, %
1.1 ± 0.4
1.0 ± 0.3
1.3 ± 0.2
0.9 ± 0.2
1.0 ± 0.1
QR
$
The Ermakovo climatype of Siberian pine is a local climatypes, i.e. growing in ecosystems adjacent to the field experimental plots
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Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil
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Table 4. Results of the univariate and multivariate ANOVA for soil microbiological properties
under Siberian pine: factor contribution into the total variance (%) and
significance level
Variate
Pine climatype
(A)
SMBС
3 (0.89)
SMBN
27 (0.03)
SMB С/N
16 (0.43)
CO2
4 (0.52)
SIR
36 (0.16)
QR
3 (0.51)
Qmet
1 (0.96)
SMBC/SOC
4 (0.87)
SMBN/SON
30 (0.09)
All variates
(0.04)
Note: values P ≤ 0.05 are shown in bold.
Factor
Soil
(B)
9 (0.45)
51 (0.00)
7 (0.39)
75 (0.00)
2 (0.63)
73 (0.00)
1 (0.95)
3 (0.66)
39 (0.02)
(0.08)
Interaction
(A x B)
5 (0.85)
26 (0.04)
17 (0.41)
1 (0.84)
45 (0.10)
12 (0.11)
3 (0.90)
4 (0.87)
23 (0.14)
(0.04)
Table 5. Results of the univariate and multivariate ANOVA for soil microbiological properties
under Korean pine: factor contribution into the total variance (%) and
significance level
Factor
Soil
(B)
Variate
Pine climatype
(A)
SMBС
7 (0,58)
17 (0,40)
3 (0,72)
SMBN
18 (0,08)
63 (0,01)
19 (0,07)
SMB С/N
1 (0,93)
54 (0,09)
1 (0,76)
CO2
40 (0,00)
49 (0,00)
25 (0,02)
SIR
19 (0,34)
9 (0,50)
1 (0,99)
QR
27 (0,01)
62 (0,00)
21 (0,02)
Qmet
16 (0,09)
70 (0,01)
7 (0,22)
SMBC/SOC
1 (0,91)
72 (0,03)
1 (0,94)
SMBN/SON
11 (0,09)
76 (0,00)
13 (0,07)
All variates
(0,19)
(0,14)
(0,21)
Note: values P ≤ 0.05 are shown in bold.
Interaction
(A x B)
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Thus such soil microbial properties as respiratory activity and absolute and relative
microbial biomass nitrogen content, found to be the most susceptible to physiological and
biochemical peculiarities of climatypes, pertain to organic matter mineralization and nitrogen
immobilization. Earlier in experiments with another pine species, Pinus sylvestris L., we found
the effect of climatypes on SMBC contribution into SOM and on SMB C/N ratio . [34], i.e. on
soil microbial properties related to microbial utilization efficiency and availability of organic
substrates. This difference in sets of parameters, responsive to the effect of intraspecies
heterogeneity of trees, can partially result from the difference between species, as well as from
the fact, that geographically and pedologically the experiment with the Scots pine was much
broader, embracing three different locations in Western and Central Siberia and four different
soils.
Pine growth and soil microbiological properties
Principal components analysis of the data matrix with tree growth and development
parameters (tree height and its annual increment, trunk and crone diameters, and branching
pattern) as variables for analysis and soil microbial properties as supplementary variables
visualized the structure of relationships among the variables, on one hand, and tree climatypes
and species, on the other hand (Fig. 1). Clear differentiation of pine species according to their
growth and development parameters is positively correlated with soil microbial biomass C/N
ratio and SIR. Judging by tree height, its annual increment, trunk and crone diameters, Korean
pine, despite the non-native soil and climatic environment, has been growing much better as
compared to Siberian pine [35], hence uptaking more nitrogen from soil, which results in its
relatively less availability fоr microbial immobilization. The latter, it its turn, results in decreased
metabolic activity [36] and increased microbial biomass C/N ratio. Additionally, pine phytomass
also differs in its chemical composition, which may also affect microbial biomass C/N ratio. As
for SIR, its negative correlation with tree growth and development parameters (Fig. 1), and
therefore with plant litter and rhizodeposition, proves less availability of carbon substrates for
microbial utilization in soil under Siberian pine, explaining the stated above more pronounced
response of soil microorganisms to substrate addition (Tabs. 1, 2).
The intraspecies variability of growth and development parameters of both pine species
was related to soil basal respiration and respiratory quotient, i.e. the ratio of active to potentially
active microorganisms: the taller the trees and the more intensively they grow, the higher the
microbial metabolic activity in the soil underneath (Fig.1). And, vice versa, the shorter and less
Makarikova R., Naumova N., Kuznetcova G. Intra- and interspecies variability of pines: relationship with soil 10
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developed the trees, the lower soil microbial metabolic activity, but, due to the correspondingly
decreased uptake by trees, more microbially immobilised nitrogen and higher its contribution
into the total soil nitrogen.
Figure 1. Projection of microbiological properties and climatypes on the plane of the first two
principal components, extracted from the data matrix with tree growth and development
parameters as variables and climatypes as objects. Active variables: Hei, tree height; Inc,
annualheight increment; Dia, trunk diameter; Cro, crone diameter; Bra, branching pattern.
Supplementary variables (*) are denoted as in Table 1. Climatypes of Siberian pine: Е,
Ermakovo; К, Kemerovo; T, Tomsk. Climatypes of Korean pine; Kh,
Khabarovsk; P,
Primorsk.
Conclusions
In the 30 years old artificial phytocoenoses the growth and development of pine trees was
found to influence some soil microbiological properties. Bigger height and its annual increment,
as well as trunk and crone diameters of Korean pine apparently led to increased input of its plant
material on/into soil and, consequently, to more comfortable environment for soil
microorganisms and their less pronounced response to the addition of easily available substrates
to bulk soil. In the rhizosphere soil the interspecies pine heterogeneity affected soil microbial
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biomass carbon and its contribution into soil organic carbon. As for the intraspecies pine
heterogeneity, Siberian pine climatypes influenced soil microbial biomass nitrogen and its
contribution into total soil nitrogen, whereas Korean pine climatypes affected soil basal
respiration and respiratory quotient.
The clear differentiation of the pine species according to their growth and development
was positively correlated with soil microbial biomass C/N ratio and SIR, whereas tree growth
and development of climatypes of both species were mostly related to soil basal respiration and
absolute and relative microbial biomass content.
Overall at the studied stage of phytocoenoses development the variability of soil
microbiological properties due to the immediate effect of pine roots, significantly exceeds the
variability caused by the inter- and intraspecies heterogeneity of pine physiology, biochemistry
and productivity. Therefore the structure and development of plant root systems should be
targeted specifically both in soil ecological studies and technological practices, involving woody
plants.
Acknowledgements
The study was supported by the Russian Foundation of Basic Research (grant No.13-0401671) and project VI.54.1.4. «Biological and biogeochemical functions of soils as a component
of terrestrial ecosystems in Siberia» (state registration No. 01201350243).
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Citing:
Naumova N., Makarikova R., Kuznetsova G. Intra- and interspecies variability of pines:
relationship with soil chemical properties in the long-term provenance experiment in the Western Sayans
// AgroEcoInfo. – 2014, N 3. http://agroecoinfo.narod.ru/journal/STATYI/2014/3/st_12_eng.doc.