Ecological Indicators 126 (2021) 107670

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Afforestation affects soil seed banks by altering soil properties and

understory plants on the eastern Loess Plateau, China
Yao Zhao a, Meng Li b, Jiayong Deng a, Baitian Wang a, c, *
a
Key Laboratory of State Forestry Administration on Soil and Water Conservation, School of Soil and Water Conservation, Beijing Forestry University, Beijing 100083,
China
b
National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China
c
Forest Ecosystem Studies, National Observation and Research Station, Jixian, Shanxi 042200, China

A R T I C L E I N F O A B S T R A C T

Keywords: To solve the serious soil erosion problem on the Loess Plateau, large-scale reforestation efforts have been carried
Plantations out in the past few decades. However, previous studies on the species diversity of these reforestation plantations
Soil properties focused mainly on the aboveground vegetation while ignoring the value of soil seed banks for diversity con­
Understory vegetation
servation. An understanding of the determinants of the soil seed banks is particularly lacking. We investigated
Soil seed bank
Diversity
the compositional characteristics of understory plants and soil seed banks in rehabilitation areas with different
vegetation types in the Caijiachuan watershed in Shanxi, China. The results indicated that the understory
vegetation and soil seed banks differed significantly among the different vegetation types. The rehabilitation
effect of plantations was significantly better than that of naturally restored abandoned farmland, while the se­
lection of afforestation tree species was also crucial. In this respect, coniferous forests (Pinus tabulaeformis) were
not as effective as broad-leaved forests (Robinia pseudoacacia) and mixed coniferous-broad-leaved forests in terms
of vegetation recovery. In addition, there were significant differences between the composition of the seed bank
and the actual vegetation, but the soil seed banks in the plantations may nonetheless contribute to the recon­
struction of the aboveground vegetation; the R. pseudoacacia forest and mixed forest showed greater regeneration
potential from the seed bank. Afforestation significantly affected the composition and structure of the understory
plant and seed banks by altering the understory habitat. Correspondingly, we inferred that afforestation may
restrict the development of understory plants and seed banks mainly by regulating soil moisture and canopy
density. Therefore, in vegetation communities with high afforestation density or canopy density, measures such
as thinning or pruning should be implemented to provide suitable habitat for understory plant growth and seed
germination. In addition, most plantations in this area are composed of a single tree species, so we suggest that
human interventions to promote the conversion of single-species plantations to diversified or uneven-aged forests
should be performed.

1. Introduction vegetation rehabilitation measures have been implemented to prevent

Soil erosion is the main cause of land degradation and ecosystem
imbalances and has become one of the most serious eco-environmental
problems in the world (Pimentel and Kounang, 1998). The Loess Plateau
is a typical soil erosion-prone area because of its loose soil, low erosion
resistance and concentrated and high-intensity rainfall patterns (Zhao
et al., 2013). However, due to severe soil water and nutrient losses, the
spontaneous restoration process of plant communities on the Loess
Plateau occurs very slowly (Zheng et al., 2005). Therefore, many
soil erosion and promote ecological restoration in recent decades (Luo
et al., 2019; Dou et al., 2020). Through afforestation, the habitat envi­
ronment and soil properties can be improved, which accelerates the
recovery of undergrowth vegetation (Dou et al., 2020; Zhao et al., 2020),
thereby effectively preventing soil erosion (Wang et al., 2016; Liu et al.,
2020). To achieve this goal, a large number of tree species used for soil
and water conservation that exhibit drought and barrenness tolerance
and strong adaptability, such as Pinus tabulaeformis and Robinia pseu­
doacacia, have been planted on the Loess Plateau to promote rapid

* Corresponding author at: Key Laboratory of State Forestry Administration on Soil and Water Conservation, School of Soil and Water Conservation, Beijing
Forestry University, Beijing 100083, China.
E-mail address: wbaitian@bjfu.edu.cn (B. Wang).

https://doi.org/10.1016/j.ecolind.2021.107670
Received 15 December 2020; Received in revised form 16 March 2021; Accepted 28 March 2021
Available online 7 April 2021
1470-160X/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Y. Zhao et al.
ecosystem recovery. Numerous studies have shown that the ability of
forest land to control soil erosion is significantly better than that of
grassland and cultivated land (El Kateb et al., 2013; Wang et al., 2013;
Liu et al., 2020).
Changes in understory habitat caused by afforestation can lead to the
emergence or disappearance of various plants under the forest canopy;
therefore, many studies have been performed on the improvement or
decline of biodiversity in the plantations in this area (Wang et al., 2014,
2019; Zhao et al., 2020). However, previous studies on plant diversity in
plantations have focused mainly on aboveground vegetation while
ignoring the protective value of the soil seed bank. By storing seeds in
soil, the soil seed bank can retain important genetic information about
the plant community succession history and provides a propagule
resource for the potential regeneration of aboveground vegetation
(Smith et al., 2002; Boedeltje et al., 2003). In addition, the soil seed
bank, which stores both transient and persistent species in the
ecosystem, can help maintain the species diversity of the plant com­
munity despite vegetation degradation caused by natural or human
disturbance (Thompson, 2000). In particular, Kalamees et al. (2012)
found that compared with instantaneous seed banks, persistent seed
banks, which are regarded as “reserves of genetic potential”, are of
greater significance in ecosystem restoration and management and
could promote the regeneration of species that have gone extinct in the
aboveground vegetation (Csontos and Tamás, 2003). Thus, revealing the
structural characteristics of soil seed banks and their relationship with
aboveground vegetation is of great significance for understanding their
role in ecological restoration.
The species composition of the soil seed bank governs the distribu­
tion pattern of aboveground plant communities to some extent (Liu
et al., 2014; O’Donnell et al., 2016). Studies have indicated that soil seed
banks provide important seed resources for plant reproduction and play
an important role in the early vegetative restoration of abandoned
farmland and grassland (Ma et al., 2019; Wang et al., 2020). Specifically,
many pioneer species in the soil seed bank effectively promote the rapid
establishment of the herbaceous layer in the early stage of afforestation
or after external interference (Van Calster et al., 2008). In turn, the
succession process of the plant community significantly affects the
development of the soil seed bank, which is mainly manifested by the
fact that the composition of the soil seed bank may change with the
continuous renewal of aboveground vegetation (Wang et al., 2011a).
Numerous studies have shown that afforestation promotes the coloni­
zation and reproduction of native and exotic species, thereby increasing
the scale of the soil seed bank (Zamora and Montagnini, 2007; Wang
et al., 2017). Simultaneously, as plantations grow and develop, species
that once existed ubiquitously on the ground may gradually disappear,
creating new opportunities for the establishment of species that are
already in the seed bank but not yet widely distributed in the above­
ground vegetation (Zamora and Montagnini, 2007).
Previous studies have shown that the compositional characteristics
of soil seed banks are largely driven by aboveground vegetation, soil
properties, and various other environmental factors (Ma et al., 2017;
Erfanzadeh et al., 2020; Horáčkováet al., 2019; Ma et al., 2020) that may
affect the evolutionary history of seed banks. In some areas, continuous
agricultural activities have led to an ongoing decrease in indigenous
species in the soil seed bank as they are gradually replaced by farmland
weeds (Bekker et al., 1997; Andreasen et al., 2018). Pellissier et al.
(2008) found that variations in the soil environment, such as soil
nutrient concentration changes or salinization, could affect the
dormancy period or viability of seeds, thus affecting the germination
rate or survival rate of seeds in the soil. Additionally, changes in habitat
conditions may lead to the continuous degradation, replenishment and
regeneration of aboveground vegetation and seed banks, just as many
plants that cannot tolerate high canopy density have difficulty surviving
on the ground and thus spread their seeds in the soil (Kozlowski, 2002;
Luo et al., 2019). Hence, considering the importance of soil seed banks
in promoting vegetation restoration and maintaining species diversity, it
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Ecological Indicators 126 (2021) 107670
is necessary to study how the species assemblies of seed banks are driven
by environmental factors (Faist and Collinge, 2015).
Many studies have described the importance of the vegetation
regeneration potential of seed banks in plant community restoration
(Shang et al., 2016; Wang et al., 2015, 2019), but knowledge about the
determinants of soil seed bank composition and change is still limited. In
particular, it is not clear how plantations regulate the changes in soil
seed banks on severely degraded loess slopes. Therefore, to better un­
derstand the impact of plantations on biodiversity conservation, we
investigated the characteristics of the variations in aboveground plants
and soil seed banks in rehabilitation areas with different vegetation
types. The objectives of our study were to (1) reveal the species
composition and structure of the understory vegetation and the soil seed
bank in the different vegetation types; (2) analyse the relationship be­
tween the soil seed bank and aboveground vegetation and its potential
role in ecological restoration; and (3) determine the direct and indirect
effects of soil environmental changes caused by afforestation on the
understory vegetation and seed bank. This study may contribute to
increasing our understanding of the impact of afforestation on vegeta­
tion rehabilitation and of trends in the development of understory plant
diversity and provide a basis for formulating effective and sustainable
management strategies for the ecological restoration of plantations in
areas with severe soil erosion.
2. Materials and methods
2.1. Study area
The study area is located in the Caijiachuan watershed
(36◦ 14′ ~36◦ 18′ N, 110◦ 39′ ~110◦ 47′ E) in Jixian County, Shanxi Prov­
ince (Fig. 1). The landform is a typical gully area of the Loess Plateau,
and the terrain is high in the east and low in the west, with an elevation
of 903–1568 m. The watershed has a warm temperate continental
climate with an average annual temperature of 10 ◦ C and an average
annual precipitation of 579 mm. Precipitation is mainly concentrated in
June to September, accounting for about 70% of the annual precipita­
tion. The soil type is mainly Alfisol according to the USDA Soil Taxon­
omy. The soil has low fertility and poor erosion resistance and is thus
susceptible to serious erosion. The main tree species for afforestation are
P. tabulaeformis and R. pseudoacacia, and the stand structure is simple,
mainly artificial pure forest.
2.2. Field surveys
Large-scale afforestation was carried out in the watershed from 1993
to 1994, and the afforestation tree species were mainly R. pseudoacacia
and P. tabulaeformis. Before afforestation, the land use type was aban­
doned farmland. The plant communities in the rehabilitation areas with
different vegetation types were investigated from July to August 2019,
the peak period of plant growth (Table 1). Twenty-four representative
plots (six for each vegetation type) with similar stand densities, soil
types and terrain characteristics were selected and sampled by typical
sampling methods. Additionally, six abandoned farmlands similar to the
age of plantation were also selected. In each sample plot (20 m × 20 m),
the height and diameter at breast height (DBH) of all trees with DBH ≥ 3
cm were recorded. The canopy density was estimated by three observers
and repeated when the difference between observers was greater than
10% (Kou et al. 2016). Furthermore, three 2 m × 2 m plots were used to
investigate the understory plants in each plot. Species name, abundance,
average height and average coverage of shrubby plants (including tree
seedlings) with DBH < 3 cm and herbs were recorded. In the upper,
middle and lower positions of each sample plot, 0–10 cm soil was taken
with a cutting ring (100 cm3), weighed immediately, brought back to the
laboratory, and dried to constant weight in an oven at 105 ◦ C to
calculate the soil moisture content. The aboveground vegetation and
litter were removed prior to taking the soil sample. Since the sampling
Y. Zhao et al.
Fig. 1. Location of the study area and sampling plots (þ, Abandoned farmland; ⋆, P. tabulaeformis forest;■, R. pseudoacacia forest;▴, Mixed forest; and ●, Natural
secondary forest).
time is during the vegetation growing season, the vegetation is more
sensitive to changes in soil moisture. To further eliminate the impact of
rainfall events on soil moisture measurements, soil was collected at least
seven days after any rainfall event. These all ensure that the soil mois­
ture we measured can represent the general difference between different
plots. In the meantime, three soil samples were collected and mixed
together for the determination of soil chemical properties. Soil pH,
organic matter (SOM) and total nitrogen (TN) were determined using
the potentiometer (soil/water ratio 1:2.5), potassium dichromate and
Kjeldahl method (Lu, 2000), respectively.
2.3. Soil seed bank sampling
Since seeds are usually concentrated in the topsoil layers, soil sam­
ples (0–10 cm) were collected from all plots to analyze the species
composition characteristics of soil seed banks. In August 2019, when the
seed germination period had ended and the current-season seeds had not
yet dispersed into the soil, we collected the sustainable seed bank (Ma
et al., 2017). To reduce the edge effect, the sampling point of soil sample
was at least 1 m away from the edge of the sample plot. Before collecting
the soil, the aboveground vegetation and litter layer were removed. Six
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Ecological Indicators 126 (2021) 107670
soil cores were collected along the “S” shaped route from each plot and
mixed into one soil sample. Each soil core had a depth of 10 cm and a
width and length of 5 cm. The soil samples were placed into self-sealing
bags and sent to the laboratory for seed germination testing of the soil
seed bank.
2.4. Seed germination experiment
The soil samples were stored at a temperature of 4 ◦ C for about a
month, and then cultured in the greenhouse. The species composition
and quantity of viable seeds in soil were quantitatively analyzed by
seedling emergence method (Chaideftou et al., 2009; Bourgeois et al.,
2017). Each soil sample was sieved through a 2 mm sieve to remove
stones and plant remains. Then, the soil samples were cultured in
germination tray. In each tray, the soil samples were evenly spread on
the sterile sand soil with a thickness of no more than 2 cm, so that all
seeds had enough light and air to ensure complete germination. All trays
were watered daily to keep the soil moist. Additional protection was
provided by nylon mesh mulching to protect soil samples from foreign
seed contamination. Furthermore, to detect whether soil samples were
contaminated by foreign seeds, we set up six randomly placed control
Y. Zhao et al. Ecological Indicators 126 (2021) 107670

Table 1 Moreover, the direct and indirect effects of vegetation types, soil
Characteristics of five vegetation types on the eastern Loess Plateau. properties and understory vegetation on the soil seed bank were
Vegetation types Altitude Slope Canopy Dominant understory deduced by using a structural equation model (SEM). The SEM was
/m density species performed in Amos 21.0, and all variables except for vegetation type and
1 Abandoned 1105 21–23 0 Lespedeza bicolor, soil pH were logarithmically transformed to improve normality. The
farmland Potentilla chinensis, canopy density significantly affects the composition and distribution of
Artemisia understory plants by changing the light conditions (Tsai et al., 2018;
stechmanniana, Carex Zhao et al., 2020). Thus, according to the degree of canopy density, the
lancifolia, Viola
philippica
vegetation types were divided into five grades: 1 = abandoned farmland,
2 P. tabulaeformis 1132 19–25 0.51 Rosa xanthina, Patrinia 2 = P. tabulaeformis forest, 3 = R. pseudoacacia forest, 4 = mixed forest,
forest scabiosifolia, Artemisia and 5 = natural secondary forest.
stechmanniana,
Cynodon dactylon,
3. Results
Potentilla chinensis,
Eleusine indica
3 R. pseudoacacia 1110 18–24 0.56 Rosa xanthina, 3.1. Understory vegetation
forest Periploca sepium, Carex
lancifolia, Across all plots in our study, there were 93 species of understory
Chrysanthemum
lavandulifolium,
plants belonging to 39 families. Among them, there were 34 species of
Setaria viridis, shrubby plants (including tree seedlings) belonging to 18 families and
Artemisia 59 species of herbaceous plants belonging to 25 families. Four families
stechmanniana were shared by herbaceous and shrubby species. Asteraceae, Rosaceae,
4 Mixed forest 1126 19–24 0.60 Rosa xanthina,
Poaceae and Fabaceae were typical families in the plots, especially
Periploca sepium,
Artemisia Asteraceae, which contained 14 species that accounted for 14.89% of
stechmanniana, Carex the total species in all families. In terms of species richness, herbaceous
lancifolia, Patrinia plants dominated the composition of understory vegetation except in the
scabiosifolia natural secondary forest (Fig. 2). The species richness of understory
5 Natural 1160 21–26 0.75 Viburnum schensianum,
secondary forest Ostryopsis davidiana,
plants in all plots varied from 11 to 19 and was significantly different
Cotoneaster zabelii, among different vegetation types (F = 3.078, p = 0.038). Compared with
Forsythia suspense, abandoned farmland and P. tabulaeformis forest, the understory plants in
Carex lancifolia the R. pseudoacacia forest and mixed forest were more diverse. In
addition, the shrubby species richness of the natural secondary forest
was significantly higher than that of the other vegetation types, but its
trays containing only sterilized soil.
herbaceous species richness was the lowest.
During seed germination, seedling emergence was checked every 3
The species abundance of understory plants also differed signifi­
days, the species and quantity of seedlings were recorded, and the
cantly among the five vegetation types (F = 2.953, p = 0.040, Fig. 2),
identified seedlings were removed. The unrecognized seedlings were
being highest in the abandoned farmland and lowest in the natural
transplanted separately into additional germination trays until they
secondary forest. Similar to the species richness, the species abundance
could be identified. The tray positions were randomly redistributed
of understory plants in the natural secondary forest was the highest for
every other week to reduce the effects of light and temperature differ­
shrubby plants and the lowest for herbaceous plants. Moreover, the in­
ences caused by spatial changes on seed germination. In the later stage
dividual number of herbaceous plants of each vegetation type was much
with the low seed germination rate, the soil was out of water for about 2
higher than that of shrubby plants, by almost 8–25 times. Among the
weeks, and then irrigated twice a week and regularly loosened the soil to
understory plants of all vegetation types, Rosa xanthina, Periploca sepium
promote seed germination. After 6 months, no seedlings grew for a
and Lespedeza bicolor were the most abundant shrub species, while the
period of one month, so the germination experiment ended. In addition,
dominant species of herbaceous plants were Carex lancifolia, Patrinia
the seed density of each soil sample was represented in units of seeds per
scabiosifolia and Artemisia stechmanniana.
square meter for comparison with other studies.
The proportion of species with different life forms in the understory
vegetation varied with vegetation type (Fig. 3a). Overall, perennial
2.5. Statistical analyses herbs and shrubs were dominant in the understory vegetation. Perennial
herbaceous plants accounted for the majority of herbaceous plants
The differences in species richness, abundance and similarity of across all sampled vegetation types, followed by annual herbs. The
understory vegetation and soil seed banks among the different vegeta­ proportion of perennial herbs in abandoned farmland was the highest
tion types were analyzed using one-way analysis of variance (ANOVA). among all vegetation types and that in natural secondary forest was the
Before the ANOVA analysis, data were examined for normality and lowest. In contrast, the proportions of trees, shrubs and semi-shrubs in
homogeneity of variance, and the abundance of herbs and understory the natural secondary forest were the highest. Compared with other
plants was logarithmically transformed. The Sorenson index was used to vegetation types, annual herb species accounted for the highest pro­
assess the similarity between seed banks and understory vegetation. The portion of understory vegetation in the R. pseudoacacia forest, but shrub
calculation formula is: SI = 2 w/(a + b), where w is the number of species species accounted for the lowest proportion.
shared by understory vegetation and seed bank; a is the number of
species in understory vegetation; and b is the number of species in seed 3.2. Soil seed bank
bank. Additionally, nonmetric multidimensional scaling (NMDS) was
used to visualize the understory vegetation and seed bank data in the No seed germination was observed in the control tray, demonstrating
ordination space. Ordination was based on species abundance data, and that the soil seed bank samples were not contaminated by external seeds.
the Bray-Curtis coefficient was used to calculate the similarity matrix. In the germination experiment, a total of 54 species belonging to 33
Meanwhile, the analysis of similarities (ANOSIM) was used to test the families were identified from the germinating seeds from the soil seed
significance of the difference. The analyses were performed in R 3.5.3 banks of the five vegetation types. A few common families, such as
software. Asteraceae, Rosaceae and Poaceae, constituted the main components of

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Y. Zhao et al. Ecological Indicators 126 (2021) 107670

Fig. 2. Species richness and abundance of understory plants varied among different vegetation types. Different lowercase letters indicate significant differences (p <
0.05) among different vegetation types. Shrub, shrubby plants (including tree seedlings); Understory, shrub + herb; AF, Abandoned farmland; PT, P. tabulaeformis
forest; RP, R. pseudoacacia forest; MF, Mixed forest; NS, Natural secondary forest.

Fig. 3. Proportion of lifeform in understory vegetation (a) and seed bank (b). AH = annual herb, ABH = annual-biennial herb, BH = biennial herb, PH = perennial
herb, SS = semi-shrub, S = shrub, T = tree. AF, Abandoned farmland; PT, P. tabulaeformis forest; RP, R. pseudoacacia forest; MF, Mixed forest; NS, Natural sec­
ondary forest.

the soil seed bank; Asteraceae had the most species of all families (15
species). In addition, the species richness of the soil seed bank varied
among the different vegetation types, and the differences among the
different vegetation types were significant (F = 5.334, p = 0.003, Fig. 4).
In general, the species richness of the soil seed bank in the three plan­
tations was higher than that in the two natural restoration types.
There were significant differences in seed density among the
different vegetation types (F = 5.334, p = 0.003, Fig. 4). The seed bank
density of the R. pseudoacacia forest was significantly higher than that of
the other vegetation types, ranging from 2800 to 5400 seeds/m2
(average density of 3989 seeds/m2), followed by that of abandoned
farmland. In contrast, the seed bank density of the P. tabulaeformis forest
was significantly lower than that of the other vegetation types, ranging
from 1267 to 2800 seeds/m2, with an average density of 1911 seeds/m2.
For each vegetation type, there were 20 species whose average density
in the soil seed bank exceeded 100 seeds/m2. Of these species,
C. lancifolia, the pioneer herb species, had the highest seed density
(average 1200 seeds/m2) in the R. pseudoacacia forest.
The plant species identified in the soil seed bank were species with
different life forms. Perennial herbs accounted for 44.44% of all
germinated seeds, annual herbs accounted for 18.52%, shrubs accoun­
ted for 12.96%, and other plant life forms accounted for 24.08%. The
proportion of species with each different life form in the soil seed bank
differed among the vegetation types (Fig. 3b). The proportion of shrubs
was larger in mixed forest (16.13%) and in natural secondary forest
(16.0%) than in the other vegetation types. However, no seed germi­
nation by shrub or tree species was observed in the soil from the aban­
doned farmland. Perennial herbs clearly and significantly dominated the
germinated seeds from all vegetation types, ranging from 41.94% to
50.0% of the germinated seeds, followed by annual herbs, which ranged
from 19.35% to 26.32%.
3.3. Similarity between the soil seed bank and understory vegetation
The NMDS results showed that the species composition of the un­
derstory vegetation and the soil seed bank was significantly separated in
two dimensions according to the ANOSIM test (R = 0.7923, p = 0.001,
Fig. 5). Similarly, the overall differences in the species composition
structure of the understory plants and seed banks of all vegetation types
were significant (R = 0.7999, p = 0.001). Additionally, the differences in

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Y. Zhao et al. Ecological Indicators 126 (2021) 107670

Fig. 4. Species richness and seed density varied in soil seed banks among different vegetation types. Different lowercase letters indicate significant differences (p <
0.05) among different vegetation types. The upper and lower edges are the maximum and minimum values, respectively. The ends of the box are on the first and third
quartiles, respectively. The horizontal line in the box is the median, and the black dot is the average value. AF, Abandoned farmland; PT, P. tabulaeformis forest; RP,
R. pseudoacacia forest; MF, Mixed forest; NS, Natural secondary forest.

Fig. 5. Two-dimensional nonmetric multidimensional scaling (NMDS) ordination of species composition of understory vegetation (V1-V5) and soil seed banks (S1-
S5) (stress value = 0.1878). Numbers 1–5 represent Abandoned farmland, P. tabulaeformis forest, R. pseudoacacia forest, Mixed forest and Natural secondary forest
respectively. The location of ordination points indicates the degree of similarity.

the understory vegetation among the different vegetation types (R =
0.6448, p = 0.001) was greater than the difference between the soil seed
banks (R = 0.5194, p = 0.001).
A total of 121 vascular plant species were recorded in our study.
Approximately 54 species were found in the soil seed bank, while nearly
twice as many species (93 species) were found in the understory vege­
tation. However, only 28 species were found only in the seed bank but
not in the understory vegetation, accounting for 23.14% of the total
number of species recorded. In contrast, more than half of the total
numbers of species (67, i.e., 55.37%) were found only in the understory
vegetation. In general, the species composition of the established
vegetation in all vegetation types showed relatively low similarity to the
species composition of the seed banks, and there were significant dif­
ferences among the different vegetation types (F = 11.277, p < 0.001,
Fig. 6). Comparatively, the understory vegetation and seed bank in the
mixed forest were the most similar, followed by those of the
R. pseudoacacia forest and P. tabulaeformis forest and finally the aban­
doned farmland and the natural secondary forest. The overall trend was

6
Y. Zhao et al.
Fig. 6. The Sørensen similarity index between the understory vegetation and
seed bank in different vegetation types. Different letters indicate significant
differences of mean values. AF, Abandoned farmland; PT, P. tabulaeformis for­
est; RP, R. pseudoacacia forest; MF, Mixed forest; NS, Natural secondary forest.
that the similarity between the understory vegetation and the seed bank
in the plantations was higher than that in the two natural restoration
types.
3.4. Direct and indirect effects of vegetation types on the soil seed bank
Overall, the data was well fitted by the SEM model (χ 2 = 13.273, DF
= 8, CMIN/DF = 1.659, GFI = 0.912, CFI = 0.925, RMSEA = 0.151).
Vegetation type had no direct impact on the species richness or seed
density of the seed bank but had a direct and significant impact on the
species abundance of the understory vegetation (Fig. 7). We found that
vegetation type was significantly correlated with soil organic matter,
soil total nitrogen and soil moisture. Among them, soil total nitrogen had
a significant negative effect on the species richness of the soil seed bank.
Moreover, soil moisture significantly affected the species richness and
abundance of the understory vegetation, which in turn had a significant
positive impact on the species richness and seed density of the seed
banks.
4. Discussion
4.1. The understory plant communities and seed banks changed with
vegetation types
As expected, there were significant differences in species richness
and abundance among the different vegetation types. This may be
caused by the emergence of trees of different species that redistribute the
light and space resources of forestlands in different ways, thus affecting
the distribution of understory plants. Specifically, the species abundance
in the abandoned farmland was the highest, but the species richness was
the lowest; these findings are similar to those of Wang et al. (2017).
Additionally, although the shrubby species richness and abundance in
the natural secondary forest were the highest, the herbaceous species
richness and abundance were the lowest. We speculate that the canopy
density increases gradually with the natural succession of the secondary
forest, which significantly limits the invasion, colonization and repro­
duction of photophilous plants. Moreover, lower species richness and
abundance were found in the P. tabulaeformis plantations, which may
confirm previous studies have shown that coniferous forests are less
effective in promoting understory plant diversity than broad-leaved
forests or mixed forests (Qu et al., 2010; Yang et al., 2010; Li et al.,
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Ecological Indicators 126 (2021) 107670
Fig. 7. The structural equation model considered all plausible pathways of
direct and indirect effect of vegetation types on species richness and seed
density. Each arrow represents a causal relationship. Coefficients with P < 0.05
were considered to be significant. Some insignificant paths are hidden for the
simplicity of the model diagram. Blue and red arrows represent significant
positive and negative correlation, respectively. Multiple R2 are given above the
box of the respective response variable. VEtype, vegetation types; SOM, soil
organic matter; TN, total nitrogen; SM, soil moisture; pH, soil pH; VErichness
and VEabundance, species richness and abundance in the understory vegeta­
tion; SBrichness and SBdensity, species richness and seed density in the seed
bank. (For interpretation of the references to colour in this figure legend, the
reader is referred to the web version of this article.)
2015). Furthermore, the successional stage of a plantation community
has a significant impact on the presence of certain plant species under
specific overstory vegetation types (Horáčková et al., 2019). For
example, several representative species, namely, Chrysanthemum lav­
andulifolium, P. scabiosifolia, and Metaplexis japonica, were found only in
the R. pseudoacacia forest we studied but not in a 17-year-old
R. pseudoacacia forest (Wang et al., 2014). This could be explained by
the fact that the emergence of these species in specific vegetation and
successional stages is attributed to specific understory habitat conditions
(Rago et al., 2020).
A total of 93 species of understory plants belonging to 39 families
were recorded across all vegetation types. Among them, the represen­
tative families were Asteraceae, Poaceae, Fabaceae and Rosaceae. Many
species from naturally restored communities, such as Adenophora
wawreana, Bupleurum chinense and Peucedanum praeruptorum, were not
found in the plantations. As a result, the number of naturally occurring
species in these forests is decreasing, but this is conducive to the colo­
nization of alien and weedy species in the plantation (Piwczyński et al.,
2016). Plantations are generally considered to have lower species rich­
ness and diversity than natural forests. However, according to our data,
the artificial rehabilitation community was superior to the natural
restoration community in maintaining species diversity and regenera­
tion potential. In addition, the positive effects of afforestation on the
improvement of the understory environment and the regeneration of
local species have also been reflected in other studies (Becerra and
Montenegro, 2013; Zhao et al., 2020). Therefore, these results indicate
Y. Zhao et al.
that plantations established on degraded lands could promote the
rehabilitation of understory vegetation by enhancing the heterogeneity
of the understory environment and providing migration opportunities
for different plant species but that the differences caused by the different
tree species cannot be ignored.
In the seed germination experiment, 54 species belonging to 33
families were found in the soil seed bank. However, the number of
species with germinated seeds in the seed bank was only approximately
half that of the understory vegetation. This difference may be caused by
many seeds stored in litter layer or the limited sampling size of the seed
bank (Wang et al., 2010; Cheng et al., 2012), indicating that the actual
number of seeds in the soil seed bank may be underestimated. In addi­
tion, many species cannot form a permanent seed bank, resulting in
some species that are conspicuous in vegetation being rare in soil seed
banks (Horáčková et al., 2019). For example, P. scabiosifolia,
C. lavandulifolium and C. dactylon were widely found in aboveground
plants, but they were very rare in seed banks. Most of the species in the
soil seed bank belonged to Asteraceae, and the species of this family
were widely distributed in the soil seed banks of the different vegetation
types. For instance, several species, i.e., A. stechmanniana, Artemisia argyi
and Artemisia annua, were quite successful at seed diffusion. These
species not only produce a large number of seeds but also make use of
various diffusion mechanisms; these are two of the main reasons why
these plants are widely distributed in the area (Wang et al., 2010; Jiao
et al., 2013). Surprisingly, although only two Cyperaceae species were
identified in the seed banks, a high number of their seeds were found,
especially of C. lancifolia, which was prevalent in all vegetation types
and had the highest total number of germinated seeds.
There are significant differences in the effects of vegetation resto­
ration among different restoration patterns, and these differences lead to
differences in soil seed bank restoration (Wang et al., 2017). Plantations
can generally promote the environmental conditions required for the
establishment of understory plants, thereby recruiting more plants and
producing large quantities of seeds, which promotes the development of
soil seed banks (Zhang et al., 2017). We also found that the species
richness of the soil seed banks in the plantations was significantly higher
than that in the natural restoration types. The species richness and seed
density of the seed bank in the R. pseudoacacia forest were the highest,
while those of the natural secondary forest were lower. This may be
attributed to the fact that R. pseudoacacia has a higher crown with more
canopy gaps than other forest types, allowing more plants to invade and
produce considerable numbers of seeds. Conversely, the natural sec­
ondary forest creates a close crown that reduces the available light re­
sources, thus limiting the growth of understory plants and ultimately
reducing seed production and spread (Ida and Kudo, 2007; Yang et al.,
2010; Dang et al., 2018; Erfanzadeh et al., 2020). Additionally, some
seeds have a finite life span, so the seed bank may be depleted in the later
stages of succession (Fenner, 1992). Nevertheless, the P. tabulaeformis
forest, which had the lowest surface vegetation coverage on the ground,
had a very low average seed density; these findings may reflect the
different influences of broad-leaved and conifer species on vegetation
rehabilitation and diversity development in serious soil erosion areas. As
Chen et al. (2018) showed, the ability of P. tabulaeformis forest to control
soil erosion is lower than that of R. pseudoacacia forest and other mixed
forests.
4.2. The relationship between the seed bank and the understory vegetation
There were also differences in the plant life forms of the species in the
understory vegetation and in the soil seed banks. The understory vege­
tation tended to have shrub and perennial-herb life forms, while the
species in the seed bank tended to be perennial herbs and annual herbs.
The most obvious trend was that shrubs species accounted for a large
proportion of the understory vegetation, while in the seed banks, few of
the germinated seeds were shrub species. This may be because most
shrub seeds have difficulty penetrating the soil surface due to their shape
8
Ecological Indicators 126 (2021) 107670
and size, making them more vulnerable to predation (Gómez, 2004).
Consequently, they do not usually form a long-term and lasting seed
bank (Thompson et al., 1997). In addition, these plants may rely more on
vegetative reproduction than on sexual reproduction and may therefore
contribute little to the soil seed bank (Ma et al., 2010). In contrast,
herbaceous plants produce abundant small seeds that spread rapidly and
easily enter the soil (Douh et al., 2018). In both the understory vege­
tation and the seed bank, perennial herbaceous plants accounted for
more than 35% of the species (more than 41% in the seed bank). This is
consistent with the general law of plant geography; that is, in temperate
regions, hemicryptophytes account for a large proportion of all species
(Wang et al., 2020). Moreover, interestingly, the Gramineae in the seed
bank were all annual herbs, with no perennials. This may be because the
relatively large and flat shape of the perennial grass seeds hinders their
burial (Thompson et al., 1993). Furthermore, annual plant seeds are
more likely to escape from predators and are more persistent in the soil
than perennial plant seeds (Wu et al., 2006; Wang et al., 2011b).
The similarity between the understory vegetation and the seed bank
species was low in the study area, and there were significant differences
among the different vegetation types. Nevertheless, the similarity in
plantation forests was higher than that in the natural restoration sites,
which to a certain extent means that the soil seed bank of plantation
forests has a positive effect on the reconstruction of understory vege­
tation (Ma et al., 2019). Additionally, high diversity and density of the
soil seed banks can improve vegetation resilience, because diversified
seed banks may contain more species with strong resilience (Ma et al.,
2019; He et al., 2020). Therefore, it can be found that afforestation may
increase the vegetation regeneration potential of the seed bank. Among
them, R. pseudoacacia forest and mixed forest showed greater potential
to regenerate from the seed bank. In addition, the similarity between the
understory vegetation and the seed bank depends not only on vegetation
type, restoration status and disturbance intensity but also on succession
history (Shang et al., 2016). Simultaneously, this similarity is also
essential for evaluating the succession and stability of plant commu­
nities (Bossuyt and Honnay, 2008; Lu et al., 2010). In this regard, Ma
et al. (2017) found that the change of soil seed bank with community
succession lagged behind that of understory plant community. As
corroborated in this study, the importance of various understory vege­
tation species changes during forest development in the different vege­
tation types; some species have disappeared from the understory
vegetation, but their seeds may still be stored in the seed banks (Dev­
laeminck et al., 2005). In addition, Cassandras et al. (2007) found that
this similarity is relatively high when the soil seed bank is dominated by
annual herbaceous plants (James et al., 2007), but a high percentage of
annual plants means that a vegetation community is in the early suc­
cessional stages and has low stability (Chen et al., 2016). As succession
continues, the similarity between the understory vegetation and the seed
bank may gradually decrease; this occurs mainly because of the lack of
any disturbance in the later stages of succession that would create a new
open area for seed germination (Horáčkováet al., 2019). During this
period, the established vegetation dominated by perennials makes the
seed bank lack correlation with the understory vegetation. This pattern
is consistent with the trend of low similarity in the natural secondary
forests and plantation forests we studied. This result also corroborates
previous research reports that the similarity in a stable vegetation
community with low disturbance intensity was low (Bossuyt and Hon­
nay, 2008; Wang et al., 2020). Likewise, it may also indicate that
plantation communities tend to stabilize after more than 20 years of
development rather than experiencing plant species homogenization, as
reported in R. pseudoacacia plantations by Zhang et al. (2020).
4.3. Direct and indirect effects of different vegetation types on seed banks
Many studies have shown that climatic conditions, vegetation type,
disturbance intensity, and soil environment are important factors
affecting the driving mechanisms of soil seed banks (Ma et al., 2010,
Y. Zhao et al.
2020; Douh et al., 2018; Haight et al., 2019). We suggest that the
changes in the understory micro-habitat caused by afforestation may be
an important driving factor for the understory vegetation and soil seed
bank in this area. Previous studies on the Loess Plateau have shown that
plantations significantly promote vegetative succession, increase soil
nutrient levels, and better maintain the diversity of seed banks
compared with naturally restored abandoned land (Wang et al., 2017;
Zhao et al., 2020). Similarly, Xu et al. (2014) also believed that affor­
estation is more effective than natural grassland restoration in
increasing soil nutrient levels in areas with serious soil erosion. In this
study, the vegetation type had a significant impact on soil nutrient
levels, but the soil organic matter content had no direct significant
impact on understory vegetation or the seed bank; this lack of impact
suggests that soil organic matter may not be a limiting factor for un­
derstory plant communities in this area. In contrast, soil TN had a sig­
nificant negative correlation with the species richness of the seed bank,
which is consistent with the study of Ma et al. (2020). This result may be
due to the fact that nitrogen is an important factor restricting plant
growth, as confirmed in previous studies (Fay et al., 2015); therefore,
higher nitrogen levels may promote seed germination, thereby reducing
the species richness of the seed bank. In addition, soil pH has been re­
ported to be an important factor influencing the species richness of plant
communities (Van der Welle et al., 2003). Soil pH can indirectly affect
the seed bank by affecting the growth of understory plants (Ma et al.,
2017). However, this effect was not found in our study, possibly because
the soil type was the same in all plots and there was little variation in pH.
Previous studies have shown that the size of the persistent seed bank
increases as drought intensity increases (Cowling et al., 2005) and that
increased soil moisture stimulates seed germination (Ma et al., 2020).
However, excessively moist soil may reduce the supply of oxygen
required for seed respiration and thereby interfere with seed metabolic
processes, leading to more seeds rotting or deteriorating (Ma et al.,
2017). Therefore, an appropriate increase in soil water may directly
change the seed dissemination strategy of plants by influencing seed
dormancy and germination (Ma et al., 2020). In this study, the soil
moisture content changed significantly among the different vegetation
types and indirectly affected the soil seed bank through its influence on
understory vegetation. These results indicate that soil moisture may be
the main environmental factor driving the growth of understory vege­
tation and the accumulation and germination of seeds in this region. In
addition, increases in canopy density among the different vegetation
types (ranked from low to high canopy density, i.e., 0 to 0.75) had a
significant negative impact on the species abundance of understory
vegetation, indicating that canopy density may also be an important
factor limiting the growth of understory vegetation. Correspondingly,
Fang et al. (2018) showed that the canopy density is extremely signifi­
cantly related to the direct light, scattered light and total light under the
forest. This reveals to a certain extent that the changes in light condi­
tions caused by canopy density may be an important factor in affecting
the development of understory plant communities. Consequently, these
results indicate that the overstory community may affect the develop­
ment of understory plants and seed banks mainly through the regulation
of soil moisture, which is further intensified by the changes in light
conditions caused by canopy density. In addition, soil moisture can
affect the seed survival rate by controlling microbial activities (Bekker
et al., 1998), so the important influence of microorganisms should be
emphasized in subsequent seed bank research.
4.4. Implications for vegetation restoration
Vegetation restoration and reconstruction using soil seed banks is an
effective way to protect species diversity (Cui et al., 2016). Kaiser and
Pirhofer-Walzl (2015) argued that if there are enough viable seeds in the
soil seed bank, spontaneous vegetative restoration processes may be
more successful. On this basis, Řehounková et al. (2016) asserted that it
is necessary to generate additional disturbances aside from natural
9
Ecological Indicators 126 (2021) 107670
disturbances in the process of vegetation restoration. In this study, the
species diversity of the seed bank was significantly increased after
afforestation, especially for shrub species, which is of great significance
for improving the species composition of the seed bank and maintaining
plant diversity. The overstory tree community effectively improved the
environmental conditions for seed accumulation and germination and
plant growth by reducing solar radiation, increasing air humidity and
improving the soil environment. For example, the Poa annua and Erig­
eron canadensis, which were ubiquitous in the seed bank of various
vegetation types, were only found in the aboveground vegetation in
plantation but not in abandoned farmland, indicating afforestation
provides a more suitable habitat for seed germination and seedling
formation and thus increases plant diversity. Additionally, it may further
indicate that afforestation can promote the seed bank to achieve greater
function in vegetation regeneration. However, the significant differ­
ences between seed banks and aboveground vegetation reveals that seed
banks are not always effective for restoring aboveground vegetation
because they are often composed of only a few species, usually weeds
(Lipoma et al., 2020). Therefore, when the species replenished from the
seed bank are insufficient to restore the aboveground vegetation,
appropriate human interference should be implemented, such as
planting or introducing seed banks from other locations (Golos et al.,
2016; Rago et al., 2020), provided that the topsoil comes from suitable
donor sites (Mackenzie & Naeth, 2010; Rivera et al., 2012).
Previous studies have shown plant diversity can effectively control
soil erosion by intercepting rainfall, increasing infiltration, and stabi­
lizing soil (Wang, 2004; Wang et al., 2013, 2016). After more than 20
years of succession, the rehabilitation effect of plant diversity in plan­
tation forests has been obviously better than that of naturally restored
wastelands in this area, which indicates that the selection of suitable tree
species for afforestation in areas with severe soil erosion could help
diverse species recolonize these areas, thereby helping to reduce soil
erosion. In addition, studies have indicated that some plantation forests,
such as R. pseudoacacia forests and P. tabulaeformis forests, play an
important role in vegetation rehabilitation and reconstruction on the
Loess Plateau (Qin et al., 2017; Zhao et al., 2020). However, these
plantation forests usually consist of a single tree species, and there are
few tree seedlings under the forest. Therefore, it is necessary to promote
the transformation of single-species tree plantations into diversified or
uneven-aged plantations through human disturbance to provide more
diverse habitats for the growth and reproduction of understory plants.
Furthermore, plant communities with greater canopy openness and
frequent disturbances often form richer seed banks (Alvarez-Aquino
et al., 2005; Melo et al., 2007). In view of this, for plantations with high
tree density or high canopy density, thinning activities such as pruning
and logging should be performed to promote seed germination and
regeneration by opening tree crowns and increasing the space resources
in the understory. In general, evaluations of plant community recon­
struction or degradation usually tend to focus on understory conditions.
However, our research indicates that ecologists should also focus on the
potential contribution of soil seed banks to vegetation restoration and
protection, as well as the direct and indirect impacts of habitat changes
on soil seed banks.
5. Conclusion
This study shows that afforestation effectively promoted understory
vegetation reconstruction and maintained the species diversity of the
seed bank but that the selection of afforestation tree species was also
critical for achieving these goals. In this respect, coniferous forests
(P. tabulaeformis) were not as effective as broad-leaved forests
(R. pseudoacacia) and mixed coniferous-broad-leaved forests in terms of
understory vegetation recovery. Afforestation could increase the vege­
tation regeneration potential of the seed bank, but the species lacking in
the seed bank should be supplemented through other measures. In
addition, afforestation significantly changed the understory habitat,
Y. Zhao et al.
thus affecting the composition of understory plants and seed banks.
Given these results, we inferred that afforestation may constrain the
development of understory plants and seed banks primarily through the
regulation of soil moisture, which is further intensified by the changes in
light conditions caused by canopy density. However, most of the plan­
tations in the study area are composed of a single tree species. Therefore,
we suggest that human interventions should be applied to promote the
conversion of single-species plantations into diversified plantations,
such as plantations under close-to-natural forest management. In addi­
tion, in communities with high forest density or high canopy density,
measures such as thinning or pruning should be adopted to increase the
amount of light and space resources under the forest canopy to promote
seed germination and reproduction. In conclusion, we call on ecologists
to pay more attention to the ecological significance of soil seed banks in
vegetation restoration and ecological protection.
CRediT authorship contribution statement
Yao Zhao: Conceptualization, Methodology, Investigation, Data
curation, Visualization, Writing - original draft. Meng Li: Investigation,
Visualization. Jiayong Deng: Investigation. Baitian Wang: Conceptu­
alization, Methodology.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
This research was supported by the National Natural Science Funds
of China (No. 31971725) and the National Key Research and Develop­
ment Program of China (No. 2016YFC0501704). We acknowledge the
assistance of the Forest Ecosystem Studies, National Observation and
Research Station, Jixian, Shanxi, China, for their invaluable help in the
field experiments.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ecolind.2021.107670.
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