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Article

Effects of Topography on Radial Growth of Tree Species with Different Mycorrhizal Types

by
Yunfei Diao
1,2,3,
Su Zhang
2,
Yulong Liu
2,3,
Guangze Jin
1,
Songyan Tian
2,3 and
Yankun Liu
2,3,*
1
Center for Ecological Research, Northeast Forestry University, Harbin 150040, China
2
Research Institute of Ecology in Heilongjiang Province, Harbin 150040, China
3
Heilongjiang Mudanjiang Forest Ecosystem National Positioning Observation and Research Station, Harbin 150040, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(3), 546; https://doi.org/10.3390/f14030546
Submission received: 23 February 2023 / Revised: 2 March 2023 / Accepted: 7 March 2023 / Published: 10 March 2023
(This article belongs to the Special Issue Long-Term Monitoring of Forest Biodiversity and Dynamics in China)
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Abstract

:
In the dynamic monitoring fixed sample plot of 25 ha of coniferous broad-leaved mixed forest in the temperate zone of Northeast China, we used the data from two surveys (2013 and 2018) and microtopography data of the sample plot, and the mycorrhizal type data of tree species to explore whether the different microtopography types and single terrain factors will affect the radial growth of tree species with different mycorrhizal types on a regional scale. We studied the adaptability of tree species with different mycorrhizal types in the north end of Changbai Mountain and the south slope of Laoyeling mountain, and which provided basis for further revealing the response mechanism of tree species with different mycorrhizal types to the microtopography in this area. We found that: the tree species with different mycorrhizal types have higher radial growth rates on gentle slopes than on steep slopes. Tree species on sunny slopes have higher growth rates and survival rates than tree species of the same mycorrhizal type on shady slopes. The quantity and radial growth of AM (Arbuscular mycorrhiza) type, EcM (Ectomycorrhiza) type, and ErM (Ericoid mycorrhiza) type tree species were significantly positively correlated with different microtopography types. The quantity and radial growth of AM type tree species and EcM type tree species were significantly positively correlated with slope. The quantity of AM type tree species, EcM type tree species and the radial growth of EcM type tree species were significantly negatively correlated with slope aspect. The quantity and radial growth of ErM type tree species and radial growth of EcM type tree species the were significantly positively correlated with slope position. We believe that the reasons for these conclusions may be caused by the differences in soil temperature, humidity, and water distribution caused by different slopes.

1. Introduction

The dominant factor in the distribution of plant species, life forms, or vegetation types on a regional to global scale is the zonal climate conditions [1,2]. In hilly or mountainous areas, topography is one of the most important factors affecting the vegetation pattern in the same climate area [3], and also one of the most important environmental gradients providing habitat diversity for plant communities. Vegetation distribution is closely related to the topography pattern [4]. Topography is an important source of environmental spatio-temporal heterogeneity at different scales, controlling basic ecological factors such as light [5], temperature [6], water, soil nutrients, etc. [7,8]. Different topographies affect the dynamic change of soil water, resulting in differences in soil water content [6] and water use affects the renewal of tree species [9]; there are also differences in soil chemical composition [10] and soil microbial content [11] in different topographies, which also affects various environmental processes; the biomass and productivity change with the topography gradient [12]. Seedling regeneration is limited by water use efficiency and subsequent tree growth is affected by topography [13,14,15,16]. Seedling regeneration is significantly related to topography [17]. Among microtopography factors, slope direction is an important factor affecting tree species regeneration [18], which has indicative significance for the structure and dynamics of plant communities [19]. Topography has a significant impact on the community structure and species distribution [20], and also has an impact on the distribution of coarse wood residues and their decay grades [21]. Slope and aspect are the dominant topographic factors of grassland species distribution [22]. Topography has a significant impact on the distribution, death, and growth of shrubs [23]. Different topographic factors have different impacts on plant species diversity [6,24] and functional diversity [25]. Plant species diversity is affected by topographic factors such as altitude, slope aspect, and slope [26]. Slope position has a significant impact on species composition, plant size and stand structure [3,27,28]. Differences in species composition are also related to topography [29].
The research on the influence mechanism of topography on tree growth has attracted much attention. In different forest types, terrain has a different effects on the distribution pattern of aboveground biomass of plants, which may be caused by different combinations of water, heat, light, soil, and other environmental factors formed by different terrain diversities [30]. Different tree species have different growth performance under the same conditions [31], and the same tree species have different responses to the environment at different growth stages. Tree growth differences are jointly determined by plant functional diversity and topographic differences [32]. Individual studies [33] show that tree growth and regeneration have nothing to do with the terrain, and death is related to the terrain, but more studies believe that the terrain has a significant impact on the mean annual growth of DBH [34] (Diameter at Breast Height). Soil temperature and moisture are the main factors affecting the radial growth of tree species [35,36,37,38,39,40]. In the mountainous environment, different topographies have a significant impact on the quantity of dead, new and DBH growth of plants [33,41], the slope direction affects the growth rate [42] and survival rate of young trees, and the slope affects the growth of tree height [43]. The radial growth of plants is also significantly affected by their own size [44,45].
Mycorrhiza [46] is a symbiont formed by the combination of plant roots and fungi in the soil. According to the macroscopic morphology and anatomical characteristics, mycorrhiza can be divided into seven categories of monotrophid mycorrhiza [47]: arbuscular mycorrhiza, ectomycorrhiza, orchid mycorrhiza (OM), ericoid mycorrhiza, ectomycorrhiza, arbutoid mycorrhiza, and monotropoid mycorrhiza. Most plants can form mycorrhiza [48], but the distribution of mycorrhizal is uneven. Among them, AM (72% of the total), EcM (2% of the total), ErM (1.4% of the total), and OM (10% of the total) are four common types [49,50,51].
Mycorrhizal plants are the indicators, participants and promoters of the community succession process [52]. The benefits of mycorrhiza may depend on the type of mycorrhiza formed, especially in AM and EcM [53]. Some studies believe that the symbiotic relationship between plant roots and fungi (mycorrhiza) is an important part of plant soil feedback [54,55], because plant mycorrhizal fungi can help plants absorb soil nutrients and water, making them less sensitive to the indirect impact of competition, and directly provide protection against pathogens. EcM can produce antibiotic compounds to prevent some pathogens. Mycorrhizal types have strong biological effects on plant soil feedback [53]. EcM tree species are common in poor soil conditions, and their nutrient utilization is more conservative than AM tree species [53]. Consequently, plant-soil feedbacks may be more positive for ErM and EcM tree species relative to AM tree species, resulting in damped conspecific inhibition for ErM and EcM tree species relative to AM tree species. Therefore, mycorrhizal type may be an important factor in the regulation of temperate forest population and community structure [53]. Tree species in temperate regions are mainly EcM type and AM type, and most of their mycorrhizal types are associated with EcM fungi or AM fungi in the soil [56,57]. Up to 80% of plant nitrogen and phosphorus are provided by mycorrhizal fungi, and many plant species rely on these symbionts for growth and survival [58]. The forest dominated by EcM tree species may lead to the accumulation of organic nutrients because EcM can fix soil moisture and nutrients, reduce soil carbon respiration, and slow down soil carbon cycle [59,60,61,62]. Fungi provide nutrition and protection for plants from antagonists in exchange for sugars produced by photosynthesis [63,64,65]. EcM has a stronger protective effect on antagonists than AM. This mechanism may increase the survival rate of EcM species [63,66]. The root tissue of EcM tree species can be physically protected by the covering layer wrapped by fungi. EcM fungi have a strong ability to protect their host plants and regulate the feedback of plant-soil, resulting in high EcM population density. AM plants will produce negative plant soil feedback, so stable ecological mechanisms are easier to be found in AM plants [50]. Studies have proved that [67] AM fungi can enhance the photosynthesis and carbon nutrition of plant leaves, promote the absorption of nitrogen by plants, enhance the absorption of insoluble phosphorus by plants, promote the formation of aggregates of soil particles, and improve their water stability. More and more studies show that people realize the importance of root symbiosis to forest function.
Therefore, it is great theoretical significance to study the relationship between plant composition, radial growth, and its distribution and topography, to clarify the survival strategies of plants in different terrains, and to deeply reveal the mechanism of habitat on the formation of spatial pattern of plant communities.
However, there are few studies on the relationship between microtopography and the radial growth of tree species with different mycorrhizal types in temperate coniferous and broad-leaved mixed forests. Therefore, the relationship between the radial growth pattern of tree species with different mycorrhizal types and the microtopography pattern has not been fully understood.
We hypothesized that tree species with different mycorrhizal types have different responses to different microtopography habitats, so the radial growth of tree species with different mycorrhizal types is different. We predict that this difference is due to the difference in temperature, moisture, and nutrients determined by slope, aspect, and position due to the different microtopography habitats.
In this study, we first analyzed the mycorrhizal type data, DBH data and topographic data of 59 species in a 25 ha temperate forest dynamic sample plot in Muling, China, to explore whether different topographic conditions will affect tree growth on a regional scale. Second, we studied whether different types of mycorrhiza were involved in plant radial growth and their relationship with topography. Thirdly, we compared the response of radial growth of AM, EcM, and ErM tree species to different terrain conditions. Finally, we compared the explanation of topographic factors and mycorrhizal types on the radial growth of temperate forest species. We use these results to infer the importance of mycorrhizal type-microtopography on radial growth and its impact on temperate forest growth.

2. Materials and Methods

2.1. Area of Study

The research site (130°00′–130°28′ E, 43°49′–44°06′ N) is located in the Heilongjiang Muling Taxus cuspidata National Nature Reserve, China. This area is located in the continental monsoon climate of the north temperate zone at the mid latitude. It is located on the south slope of Laoyeling mountains. Laoyeling mountains belong to the northern mountains range of Changbai Mountain system, with a southwest northeast trend. In this area, the lowest altitude is 450 m, the highest altitude is 920 m, the annual mean temperature is −2 °C, and the annual rainfall is 440–510 mm.
The massif is mainly composed of granite, basalt, and gneiss of crystalline parent rock and some pre-Sinian metamorphic rock series. The subsoil layer is located between the topsoil and the subsoil, which is shallow. The surface black soil is very thin; The subsoil layer is brown, with a compact structure and different depths. The soil is acidic (pH 4.5–6.5). The main soil types include dark brown forest soil, swamp soil, and dark meadow soil. In terms of vegetation division in China, it belongs to the “temperate coniferous and broad-leaved mixed forest area”. The forest is dominated by Pinus koraiensis, Picea koraiensis, and Abies nephrolepi, accompanied by a variety of temperate broad-leaved species. The zonal vegetation is a coniferous and broad-leaved mixed forest dominated by Pinus koraiensis.

2.2. Methodology

In 2013, according to the dynamic sample plot construction standards of the CTFS-ForestGEO network and CForBio network, and with reference to the 50 ha sample plot of Barro Colorado Island, we set up a fixed sample plot for dynamic monitoring of temperate coniferous and broad-leaved mixed forest in the Heilongjiang Muling Taxus cuspidata National Nature Reserve, China. We had selected an area that has not been artificially operated since 1980, and the forests in this area are in the early growth stage of local dominant tree species. The topographic of the sample plot is high in the southwest, and low in the northwest and northeast. The highest altitude is 781 m, the lowest altitude is 658 m, and the height difference is 123 m (Figure 1). The sample plot area is 25 ha (500 m × 500 m).
We investigated the plant resources of the sample plots in 2013 and 2018, respectively. During the plant survey and microtopography survey, the total 500 m × 500 m area was divided into 10,000 5 m × 5 m small subplots. All the data collection and processing was done at the level of 5 m × 5 m subplots. We hang aluminum plates with numbers, measure and record the diameter at breast height (DBH) and coordinates of all plants (DBH ≥ 1 cm) in a fixed sequence, and record the species names of all plants in the sample plot, the number of trees [68].
The study species dataset uses the List of Chinese Plant Species Edition 2021 [69], and the mycorrhizal type dataset uses the FungalRoot Database [70].
The investigation is carried out according to three topographic parameters: height difference, slope direction, and slope. According to the terrain height difference, the sample plot is divided into two slope positions: upper slope position and lower slope position. The slope aspect is divided into five grades: shady slope (337.5°–67.5°), semi-shady slope (67.5°–112.5°, 292.5°–337.5°), flat land, semi-sunny slope (112.5°–157.5°, 247.5°–292.5°), and sunny slope (157.5°–247.5°). The slope is divided into seven grades: flat slope (0°–6°), gentle slope (6°–16°), slope (16°–26°), steep slope (26°–36°), sharp-steep slope (36°–41°), sharp slope (41°–46°), and dangerous slope (46° or more) [71]. According to the slope position, slope aspect, and slope of the three terrain parameters, the topography is finally divided into 58 different microtopography habitats, this plot covers 54 categories. Rules 1–54, see shown in Appendix A Table A1.
A square environmental factor matrix of 10,000 × 3 was established according to the slope position, slope direction, and slope of the microtopography habitat. The slope position assignment is: 1 represents lower slope position, 2 represents the upper slope position. The slope aspect assignment is: 5 represents the shady slope (A1), 4 represents the semi-shade slope (A2), 3 represents the flat land (A3), 2 is representative of the semi-sunny slope (A4), 1 is representative of the sunny slope (A5). The slope assignment is: 1 represents the flat slope (S1), 2 represents the gentle slope (S2), 3 represents the slope (S3), 4 represents the steep slope (S4), 5 represents the sharp-steep slope (S5), 6 represents the sharp slope (S6), and 7 represents the dangerous slope (S7).
In this study, we determined mycorrhizal associations for each tree species using the FungalRoot dataset. All tree species were classified into AM type, EcM type, and ErM type tree species. There were 59 tree species in the plot, and they were classified as AM-type tree species (30), EcM tree-type species (18), and ErM-type tree species (1). For the remained 10 tree species, we adopted the following method to determine their mycorrhizal types: at least two independent studies [72,73,74] found four species colonized by EcM fungi (Acer pictum subsp. mono, Acer ukurunduense, Ulmus davidiana var. japonica, and Ulmus laciniate) were identified them as an EcM tree species. We have also used the Soudzilovskaia provided method [75] to perform the determination of the mycorrhizal types in the data-free species. We hypothesized that EcM fungi could directly inhibit soil-borne pathogens or protect root tissues from antagonists, and we considered species known to be associated with AM and EcM fungi as EcM-type tree species [49].
Raw data were proofread and collated using Microsoft Excel 2016. The 2013 survey data and the 2018 survey data were compared and analyzed, and the mortality rate, new rate, and DBH increase were collated, and the microtopography data were processed [76,77]. We obtained the difference between these two surveys. All data were analyzed using the R software (Version 3.6.3; http://www.r-project.org/, accessed on 15 April 2022), and using “ggbreak”, “ggrepel”, “magick”, “magick”, “raster”, “corrplot”, “vengan”, “psych”, “spdep”, “spatialreg” and “ggplot2” packages. A linear model was used to analyze the relationship between radial growth and different microtopography.
Correlation analysis was used in our statistical analysis. Because we calculated the correlation between the radial growth of different mycorrhizal species and environmental factors, and the environmental factors are diverse, it is easy to have data that do not conform to the normal distribution, so the Spearman algorithm is adopted. Formulas 1, 2, 3, 4, and 5 are the relevant calculation formulas of ΔDBH, importance value, relative density, relative frequency and relative dominance.
ΔDBH = alive (DBH2018 − DBH2013 + new (DBH2018new) − dead (DBH2013death)
ΔDBH was calculated for AM, EcM, and ErM tree species, respectively, analyze the distribution and its relationship in different microtopographies. ΔDBH represents the variation of DBH of tree species. Alive (DBH2018 − DBH2013) represents the variation in DBH of the alive tree species from 2013 to 2018. New (DBH2018new) represents the DBH value of new trees in 2018. Dead (DBH2013death) represents the variation in DBH of dead tree species from 2013 to 2018.
Importance value = (relative abundance + relative frequency + relative dominance)/3
Relative density = (quantity of individuals/quantity of all plants) × 100%
Relative frequency = (frequency of individuals/sum of frequencies of all species) × 100%
Relative dominance = (sum of DBH of an individual specie in sample/sum of DBH of the species in sample) × 100%
We use the importance value [78] to indicate the relative importance of different mycorrhizal species in the sample. The importance value is an important indicator in calculating and evaluating species diversity, which represents the relative importance of plant species in the community with a comprehensive value. Density refers to the ratio of the individual number of a certain plant in a sample plot to the area of the sample plot. Frequency refers to the frequency of a species in all the samples made. Dominance refers to the sectional DBH of a plant in the quadrat divided by the area of the plot.

3. Results

3.1. Microtopographic Characteristics

According to the slope level, slope direction, and slope, the topographic is finally divided into 58 categories. The sample plot covers 54 different classes of microtopographic habitats. The plot quantity of microtopography is sorted from large to small, UA2S4(1126) > UA1S4(998) > UA1S3(889) > UA2S3(690) > LA2S3 (654) > UA1S2(505) >...> LA4S7(4) > LA5S5(2) > LA5S6(1) > LA3S1(1). The sample quantities of the top six in the quantities of microtopography account for 48.62% of the total samples.
Microtopography is divided into seven levels according to the slope value from large to small (S7 to S1). The plot quantity of microtopography is sorted from large to small, S4 (3579) > S3 (3486) > S2 (1811) > S5 (746) > S6 (211) > S1 (88) > S7 (79). The sample quantities of the top three in the quantities of microtopography by slope account for 88.76% of the total samples.
The microtopography is divided into five levels (A1 to A5) according to the slope direction. The plot quantity of microtopography is sorted from large to small, A2 (3931) > A1 (3865) > A4 (1418) > A5 (785) > A3 (1). The sample quantities of the top three in the quantities of microtopography by slope for 92.14% of the total samples. The relationship between the quantities of each microtopographic plots is shown in Figure 2.
The microtopography of this study area was mostly concentrated on the gentle slopes, the slopes, and the steep slopes of shady slopes, and semi-shady slopes, as shown in Figure 3.

3.2. Mycorrhizal Type Tree Species with Different Microtopography

From Appendix A Table A2, we can see the importance values of different mycorrhizal species in 54 microtopographies. There were 26 kinds of microtopography where the importance value of AM-type tree species was higher than that of EcM-type tree species, in 2013. There were 25 kinds of microtopography where the importance value of AM-type tree species was higher than that of EcM-type tree species, in 2018. Two surveys showed that: the dominant species of LA2S1 and UA1S1 types have changed from the AM-type tree species to the EcM type tree species; the dominant species of UA5S1 type has changed from the EcM-type tree species to the AM-type tree species; LA3S1 microtopography has only the AM type species. In the microtopography with ErM type tree species, the importance value of ErM type tree species is increasing; ErM type tree species appear in the UA2S5 microtopography.
Figure 4 shows the quantity of tree species changes, DBH sum changes, and mean DBH changes of the different mycorrhizal types of tree species. The microtopography types with the largest reduction in the quantity of AM type tree species were ranked as follows (The reduction in quantity, percentage of mycorrhizal tree species of the same type): UA1S3 (−1557, −9.20%), LA2S3 (−1509, −8.92%), UA1S4 (−1397, −8.25%), UA2S3 (−1332, −7.87%), UA2S4 (−1187, −7.01%), UA1S2 (−1035, −6.12%), LA1S3 (−1015, −6.00%), etc. The microtopography types with the largest reduction in the quantity of EcM-type tree species were ranked as follows: UA2S4 (−1148, −9.25%), UA1S4 (−1133, −9.13%), UA1S3 (−1031, −8.31%), UA2S3 (−1015, −8.18%), etc.

3.3. Tree Species of Different Mycorrhizal Types

From Figure 5 we draw the following conclusions.
In 2013, the total quantity was 126,530 trees (100%). The top three in quantity are Acer barbinerve (35,084; 27.73% of all), Corylus mandshurica (23,732; 18.76% of all), and Acer ukurunduense (10,140; 8.01% of all) accounted for 54.50% of the total quantity. AM type tree species are 40 species and 69,649 (55.05% of all) trees. The top three in quantity are Acer barbinerve (35,084; 27.73% of all), Acer tegmentosum (8293; 6.55% of all)and Syringa reticulata subsp. amurensis (6125; 4.84% of all) accounted for 71.07% of the total quantity of AM type tree species. EcM type tree species are 18 species and 56,770 (44.87% of all) trees. The top three in quantity are Corylus mandshurica (23,732; 18.76% of all), Acer ukurunduense (10,140; 8.01% of all) and Pinus koraiensis (4845; 3.83% of all) accounted for 68.20% of the total quantity of EcM type tree species. There is only one species of ErM type tree species, namely Rhododendron dauricum (107; 0.08% of all), accounting for 100% of the total quantity of ErM type tree species.
In 2018, the total quantity was 97,292 trees (100%), The top three in quantity are Acer barbinerve (26,796; 27.54% of all), Corylus mandshurica (14,991; 15.41% of all) and Acer ukurunduense (8105; 8.33% of all) accounted for 51.28% of the total quantity. AM type tree species are 38 species and 53,142 (54.62% of all) trees. The top three in quantity are Acer barbinerve (26,796; 27.54% of all), Acer tegmentosum (7103; 7.30% of all) and Syringa reticulata subsp. amurensis (4585; 4.71% of all) accounted for 72.42% of the total quantity of AM type tree species. EcM type tree species are 18 species and 43,946 (45.17% of all) trees. The top three in quantity are Corylus mandshurica (14,991; 15.41% of all), Acer ukurunduense (8105; 8.33% of all) and Pinus koraiensis (4659; 4.79% of all) accounted for 63.16% of the total quantity of EcM type tree species; There is only one species of ErM type tree species, namely Rhododendron dauricum (201, 0.21% of all), accounting for 100% of the total quantity of ErM type tree species.
In 2013, the mean DBH of the 59 tree species was 8.04 cm. The top three species in mean DBH were Populus koreana (39.85 cm), Taxus cuspidata (39.35 cm), and Populus ussuriensis (21.08 cm). Among them, the mean DBH of the AM-type tree species was 5.78 cm. The mean DBH of the EcM-type tree species was 13.44 cm. The mean DBH of the ErM-type tree species was 1.43 cm.
In 2018, the mean DBH of the 57 tree species was 9.49 cm. Among them, the mean DBH of the AM-type tree species was 6.70 cm, The mean DBH of the EcM-type tree species was 16.13 cm, and the mean DBH of the ErM-type tree species was 1.51 cm. The top three tree species in the mean DBH were Populus koreana (51.33 cm), Taxus cuspidata (40.18 cm), and Populus ussuriensis (25.04 cm).
We compared survey datas (2013 and 2018). The mean DBH of all tree species increased by 1.45 cm. The mean DBH of the remaining 57 species increased to varying degrees, except for the death of Salix matsudana and Viburnum opulus subsp. Calvescens. The top three tree species with an increase in mean DBH are Populus koreana (+11.48 cm), Juglans mandshurica (+7.43 cm), and Alnus hirsuta (+6.11 cm). These three kinds of tree species are tree species with large DBH and small quantity, and the mean DBH increase is largely due to the death of small individuals. The mean DBH of the AM type tree species increased by 0.92 cm. Except for the dead Salix matsudana and Viburnum opulus, the mean DBH of the remaining AM-type tree species increased by 1.08 cm. The mean DBH of the EcM-type tree species increased by 2.69 cm. The mean DBH of the ErM-type tree species increased by 0.08 cm.

3.4. Microtopographic Characteristics

Appendix A Table A3 shows the quantity and mean DBH of tree species with different mycorrhizal types in different microtopographies.
In 2013, the top three microtopography types in different microtopographies of AM type tree species quantity were: UA2S4, UA1S3, and UA1S4; the top three microtopography types in different microtopographies of EcM type tree species quantity were: UA2S4, UA1S3, and UA1S4; the top three microtopography types in different microtopographies of ErM type tree species quantity were: LA2S7, LA2S6, and LA1S7; the top three microtopography types in different microtopographies of mean DBH of AM type tree species were: LA5S6, UA1S7, and UA1S6; the top three microtopography types in different microtopographies of mean DBH of EcM type tree species were: LA5S6, UA1S7, and UA1S6; the top three microtopography types in different microtopographies of mean DBH of ErM type tree species were: LA1S6, UA1S3, and UA2S6.
In 2018, the top three microtopography types in different microtopography of AM type tree species quantity were: UA2S4, UA1S3, and UA1S4; the top three microtopography types in different microtopographies of EcM type tree species quantity were: UA2S4, UA1S4, and UA1S3; the top three microtopography types in different microtopographies of ErM type tree species quantity were: LA2S7, LA1S7, and LA2S6; the top three microtopography types in different microtopographies of mean DBH of AM type tree species were: LA5S6, UA1S7, and UA1S6; the top three microtopography types in different microtopography of mean DBH of EcM type tree species were: LA5S6, UA1S7, and UA4S1; the top three microtopography types in different microtopographies of mean DBH of ErM type tree species were: LA1S3, UA4S4, and UA2S5.
Figure 6 shows the different spatial distribution of different mycorrhizal species. From the distribution of the quantity of tree species with different mycorrhizal types in the sample plot: AM type tree species are mostly distributed on the slope or steep slope of low slope position, shady slope or semi-shady slope in the sample plot; EcM type tree species are mostly distributed on the slope or steep slope of upper slope position, shady slope or semi-shady slope in the sample plot; ErM type tree species are mostly distributed on the sharp slope or dangerously slope of shady slope or semi-shady slope in the sample plot.

3.5. Correlation Analysis

The correlations between the quantity of tree species with different mycorrhizal types and the different microtopography factors are as follows(Figure 7A): (1) The AM type tree species showed a very significant positive correlation with the different microtopography types and slopes, a very significant negative correlation with slope aspect, and a negative correlation with slope position; (2) The EcM type tree species showed a very significant positive correlation with the different microtopography types and slope, a very significant negative correlation with slope aspect, and a positive correlation with slope position; (3) The ErM type tree species showed a very significant positive correlation with the different microtopography types and slope position, a positive correlation with slope, and a negative correlation with slope aspect.
The correlations between the radial growth amount of the different mycorrhizal type tree species and the different microtopography factors are as follows(Figure 7B): (1) The AM type tree species showed a very significant positive correlation with the different microtopography types and slope, a positive correlation with slope position, and a negative correlation with slope aspect; (2) The EcM type tree species showed a very significant positive correlation with the different microtopography types, slope position, and slope, and a significant negative correlation with slope aspect; (3) The ErM type tree species showed a very significant positive correlation with the different microtopography types and slope position, a positive correlation with slope, and a negative correlation with slope aspect.

4. Discussion

We compared survey data (2013 and 2018). The quantity of AM-type tree species decreased by two species, namely Salix matsudana and Viburnum opulus subsp. calvescens Sugim, respectively. The quantity of each species in AM type tree species and EcM type tree species is decreased by different ranges, except that the quantity of the Malus baccata (AM type tree species) has not changed. The quantity of Rhododendron dauricum (ErM type tree species) has increased by 87.85%. The quantity of deaths of the top three tree species were Corylus mandshurica (8741), Acer barbinerve (8288), and Acer ukurunduense (2035), accounting for 29.99%, 28.44%, and 6.98% of the total quantity of 29,144 deaths, respectively, accounting for 65.41% in total deaths trees. The top three population that have decreased in quantity in the community were Corylus mandshurica (−3.35%), Aralia elata var. glabrescens (−0.83%), and Eleutherococcus senticosus (−0.67%). The top three trees proportion that have increased in the community were Pinus koraiensis (0.96%), Abies nephrolepi (0.79%), and Acer tegmentosum (0.75%).
Among the different microtopography types, the dominant microtopography type of AM type tree species changed from 26 microtopography types in 2013 to 25 microtopography types in 2018. LA2S1 and UA1S1 types microtopography become microtopography dominated by EcM type tree species. UA5S1 type microtopography becomes the microtopography dominated by AM type tree species. Among the 54 microtopography types, the importance value of AM type tree species in 14 microtopography types showed an upward trend, and the importance value of AM type tree species in 39 microtopography types showed a downward trend. There are only AM type tree species in LA3S1 microtopography type, so the importance value of AM type tree species in this microtopography type has not changed.
There is no increase in the quantity of AM type tree species in all microtopography types, among which there is no change in the quantity of AM type tree species in LA3S1, LA5S5,LA5S6, and UA1S7, and there is a decrease in the quantity of AM type tree species in other microtopography types. The quantity of EcM type tree species in UA5S6 microtopography show an increasing trend. The quantity of EcM type tree species in LA3S1, LA5S5, LA5S6, LA2S7,LA4S7 and LA1S7 microtopographies do not change, and the quantity of EcM type tree species in other microtopographies show a decrease. The quantity of ErM type tree species in UA1S4 microtopography decreased, and the quantity of ErM type tree species in 11 microtopographies of other ErM type tree species increased.
The increase or decrease of the quantity of different mycorrhizal types tree species in different microtopography leads to the increase or decrease of their DBH in this microtopography. The death of the tree species with small DBH in AM and EcM types tree species led to the increase of the mean DBH of different mycorrhizal types tree species in this microtopography. Due to the small quantity of ErM type tree species, the death or even disappearance of ErM type tree species in individual microtopography leads to the reduction of the mean DBH of ErM type tree species in this microtopography.
AM type tree species and EcM type tree species have higher radial growth rates on gentle slopes than on steep slopes. On the one hand, gentle slopes tend to accumulate more canopy litter than steep slopes, which is an important source of soil organic matter and nutrients; on the other hand, the surface runoff on gentle slopes is smaller than that on steep slopes, which can intercept more precipitation. The increase of soil moisture content will not only provide water for plants, but also accelerate the decomposition of humus and increase soil organic matter and soil nutrients, which is consistent with the conclusions of other studies [79,80,81].
Slope aspect affects the composition and distribution of plant species in the community by affecting light, temperature, and soil nutrients [82]. This study believes that plants located on the sunny slope have higher growth rate and survival rate than plants of the same mycorrhizal type located on the shady slope, which is contrary to the conclusion of the study [33,83], and this difference may be caused by latitude differences. Of course, the early growth of trees in a mountainous environment is species-specific, that is, trees of different species or groups behave differently in the same environment [84]; moreover, even the same plant individual may have different or even contrary reactions to the same environmental changes at different stages of growth [32,37].
The growth rate of plants is largely determined by their own individual size, so it is often expressed as a function of plant individual size [84,85], and the type of function also varies among different species. For example, the radial growth rate of Taxus cuspidata increases with the increase of DBH, showing a positive correlation [44,45]. In the process of changing from upper slope position to lower slope position, the mean tree height, mean DBH, and the proportion of individual species at higher height and DBH levels of different mycorrhizal types tree species decreased, and the species diversity showed an increasing trend. This conclusion of this study is consistent with other studies [19].
The quantity and radial growth of AM type tree species were significantly positively correlated with different microtopography types and slope, and the quantity of AM type tree species was significantly negatively correlated with slope aspect. The quantity and radial growth of EcM type tree species were significantly positively correlated with different microtopography types and slope, the quantity and radial growth of EcM type tree species were significantly negatively correlated with slope aspect, and the radial growth of EcM type tree species was significantly positively correlated with slope position. The quantity and radial growth of ErM type tree species were significantly positively correlated with different microtopography types and slope position.
In this study, the species composition, radial growth of different mycorrhizal species and the relationship between their distribution and topography were studied in detail. This has important theoretical and guiding significance for further elucidating the survival strategies of plants in different terrains and further revealing the mechanism of habitat on the formation of spatial pattern of plant communities. It should be noted that different microtopographics have a significant impact on the radial growth of plants in the temperate plant communities in the northern hemisphere. This study only examined the northern temperate forests in a small area. Due to the differences in the study scale and study area, the effects of topographic factors on the distribution and growth of different mycorrhizal types tree species are different, and the conclusions still have limitations.

5. Conclusions

In this study, the study area was divided into different microtopography habitats according to slope position, slope aspect, and slope, and the effects of microtopography on the quantity and DBH growth of different mycorrhizal types in north temperate forests were studied. The results showed that there were differences in the quantities changes and radial growth of different mycorrhizal types tree species under different microtopographies in the 25 ha fixed monitoring sample plot of coniferous and broad-leaved mixed forest in the north temperate zone in the Taxus cuspidata National Nature Reserve in Muling, Heilongjiang Province. The microtopography type is the main factor affecting the quantity and radial growth of different mycorrhizal types tree species; slope is the main factor affecting the quantity and radial growth of AM type tree species and EcM type tree species; slope aspect is the main factor affecting the quantity of AM type tree species and EcM type tree species, and the radial growth of EcM type tree species; slope position is the main factor affecting the radial growth of EcM type tree species and ErM type tree species, and the quantity of ErM type tree species.

Author Contributions

Conceptualization, Y.D.; data curation, Y.D.; formal analysis, Y.D. and S.Z.; funding acquisition, Y.L. (Yankun Liu); investigation, Y.D. and Y.L. (Yulong Liu); methodology, Y.D.; project administration, Y.L. (Yankun Liu); resources, S.T.; software, Y.D.; supervision, S.T.; validation, S.Z.; visualization, Y.D.; writing—original draft, Y.D.; writing—review and editing, G.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the following projects: 1. Keypoint research and development program of Heilongjiang Province of China, grant number GA21C030; 2. Scientific research funds of Heilongjiang provincial research institutes, grant number CZKYF2021B006; 3. Special investigation of China’s national science and technology basic resources, grant number 2019FY202300.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table
Table A1. Microtopography Classification.
Table A1. Microtopography Classification.
Upper Slope Position (U)Lower Slope Position (L)
Shady Slope
A1		Semi-Shady Slope
A2		Flat Land
A3		Semi-Sunny Slope
A4		Sunny Slope
A5		Shady Slope
A1		Semi-Shady Slope
A2		Flat Land
A3		Semi-Sunny Slope
A4		Sunny Slope
A5
flat slope
S1		UA1S1(31)UA2S1(30)UA3S1 *UA4S1(29)UA5S1(28)LA1S1(4)LA2S1(3)LA3S1(2)LA4S1(1)LA5S1 *
gentle slope
S2		UA1S2(35)UA2S2(34) UA4S2(33)UA5S2(32)LA1S2(8)LA2S2(7) LA4S2(6)LA5S2(5)
slope
S3		UA1S3(39)UA2S3(38) UA4S3(37)UA5S3(36)LA1S3(12)LA2S3(11) LA4S3(10)LA5S3(9)
steep slope
S4		UA1S4(43)UA2S4(42) UA4S4(41)UA5S4(40)LA1S4(16)LA2S4(15) LA4S4(14)LA5S4(13)
sharp-steep slope
S5		UA1S5(47)UA2S5(46) UA4S5(45)UA5S5(44)LA1S5(20)LA2S5(19) LA4S5(18)LA5S5(17)
sharp slope
S6		UA1S6(51)UA2S6(50) UA4S6(49)UA5S6(48)LA1S6(24)LA2S6(23) LA4S6(22)LA5S6(21)
dangerously slope
S7		UA1S7(54)UA2S7(53) UA4S7(52)UA5S7 *LA1S7(27)LA2S7(26) LA4S7(25)LA5S7 *
NOTE: U: upper slope position, L: lower slope position, A: slope aspect, S: slope, *: This sample plot does not cover this type.
Table
Table A2. Importance values of tree species with different mycorrhizal types in different microtopographies.
Table A2. Importance values of tree species with different mycorrhizal types in different microtopographies.
MicroreliefAM Tree SpeciesEcM Tree SpeciesErM Tree Species
2013.
Importance Value		2018.
Importance Value		2013.
Importance Value		2018.
Importance Value		2013.
Importance Value		2018.
Importance Value
LA1S152.0655.8847.9444.12--
LA1S255.5356.0144.4743.99--
LA1S355.5755.5144.4344.49--
LA1S452.4352.0747.5747.93--
LA1S539.6540.7348.9747.5811.3711.69
LA1S639.3240.3649.4048.3611.2811.28
LA1S739.4237.0045.4944.7115.0918.29
LA2S153.6745.9846.3354.02--
LA2S255.2155.0344.7944.97--
LA2S354.5254.1145.4845.89--
LA2S446.6144.9042.2243.9211.1711.18
LA2S539.7439.0549.0449.6511.2211.30
LA2S635.5033.4251.4952.0013.0114.58
LA2S741.5138.6643.6141.8214.8719.52
LA3S1100.00100.00----
LA4S169.8665.6430.1434.36--
LA4S254.7053.7845.3046.22--
LA4S357.7857.4742.2242.53--
LA4S448.4947.8051.5152.20--
LA4S538.4837.0961.5262.91--
LA4S637.5537.4650.9550.9611.5011.57
LA4S742.3041.9357.7058.07--
LA5S262.2363.7937.7736.21--
LA5S363.8563.5736.1536.43--
LA5S458.5958.5241.4141.48--
LA5S536.3036.1763.7063.83--
LA5S631.8931.9868.1168.02--
UA1S150.4049.1149.6050.89--
UA1S254.7054.3245.3045.68--
UA1S347.6547.1941.2241.6811.1211.13
UA1S444.9744.7943.8944.0711.1411.14
UA1S546.4645.9453.5454.06--
UA1S642.1840.9857.8259.02--
UA1S747.6048.2752.4051.73--
UA2S153.5457.4246.4642.58--
UA2S251.2951.7948.7148.21--
UA2S352.9152.8847.0947.12--
UA2S442.0341.9546.8246.8811.1511.17
UA2S546.1840.3953.8248.48-11.13
UA2S639.3338.9849.2948.7111.3712.31
UA2S745.1044.4943.3043.0911.5912.42
UA4S148.1249.5151.8850.49--
UA4S249.8248.6850.1851.32--
UA4S344.6546.4744.2342.3911.1211.14
UA4S441.8641.2547.0047.6011.1411.15
UA4S539.1937.6149.4450.5811.3711.81
UA4S646.4246.6253.5853.38--
UA4S745.7144.0854.2955.92--
UA5S149.0050.6351.0049.37--
UA5S243.2843.1556.7256.85--
UA5S347.2047.1952.8052.81--
UA5S453.5653.8346.4446.17--
UA5S547.5647.5152.4452.49--
UA5S670.0868.2329.9231.77--
Table
Table A3. The quantity and mean DBH of tree species with different mycorrhizal types in different microtopographies.
Table A3. The quantity and mean DBH of tree species with different mycorrhizal types in different microtopographies.
20132018
Micro-
topography		AMEcMErMAMEcMErM
QuantityMean DBHQuantityMean DBHQuantityMean DBHQuantityMean DBHQuantityMean DBHQuantityMean DBH
LA1S11852.24 1313.48 1562.61 794.91
LA1S240583.25 23604.88 31553.99 17196.42
LA1S345323.47 25295.62 35174.19 18857.40
LA1S426633.65 17366.37 21314.27 13668.06
LA1S53853.63 4105.67 51.24 3314.18 3137.13 91.39
LA1S61383.68 1258.46 12.00 1304.09 1109.45 11.30
LA1S7684.25 735.40 141.46 654.59 736.04 271.49
LA2S11202.91 715.30 653.53 645.97
LA2S235003.19 19915.20 25604.03 14336.93
LA2S360903.49 37075.43 45814.32 27996.99
LA2S427643.76 18296.55 61.38 20894.58 15507.83 61.57
LA2S53973.70 3817.16 21.40 3284.42 3318.39 31.47
LA2S61363.65 1766.01 141.59 1074.32 1556.93 231.60
LA2S7983.63 815.99 171.33 973.89 816.68 421.43
LA3S142.70 43.38
LA4S1604.63 109.84 306.22 713.83
LA4S24244.39 2915.28 3005.55 2136.97
LA4S312613.72 6784.95 9324.59 4966.47
LA4S49383.47 7257.01 7294.23 5888.55
LA4S5684.41 1038.43 555.37 959.53
LA4S6503.81 557.28 11.30 424.72 478.77 11.70
LA4S7205.52 2310.99 196.14 2311.54
LA5S22384.20 945.73 1775.60 608.26
LA5S36204.21 1748.63 4535.24 12012.29
LA5S43654.96 1916.29 2606.39 1397.83
LA5S5111.90 148.54 111.94 148.96
LA5S6211.90 523.10 212.15 523.14
UA1S11523.16 1234.60 1103.83 926.10
UA1S240473.38 23805.49 30124.05 17706.90
UA1S364123.81 41716.08 31.90 48554.54 31407.75 32.23
UA1S461143.96 46196.50 71.26 47174.75 34868.33 61.42
UA1S54804.96 4648.18 3855.95 3879.67
UA1S6655.93 7711.27 566.99 7512.07
UA1S7236.54 1912.90 236.99 1814.14
UA2S1825.05 645.41 715.84 407.42
UA2S214523.88 10596.24 11224.67 7588.22
UA2S351143.96 34716.03 37824.80 24568.01
UA2S465054.21 57467.24 121.56 53184.94 45988.95 141.69
UA2S518054.39 17677.31 15085.17 14998.58 11.80
UA2S64634.65 4907.65 61.60 4165.23 4358.73 261.47
UA2S71944.60 1447.46 41.33 1595.23 1139.41 91.52
UA4S1354.30 307.36 305.28 248.75
UA4S210503.23 7646.24 7483.95 5777.81
UA4S327483.88 22165.25 11.20 20164.83 14457.34 21.55
UA4S424594.18 21357.61 31.50 19435.02 17339.33 31.97
UA4S58464.29 8508.04 111.26 6645.11 7299.54 251.39
UA4S61855.14 1857.95 1476.19 14110.16
UA4S7373.55 318.73 294.07 2610.82
UA5S1613.57 545.14 483.99 366.56
UA5S210413.18 11076.54 7783.83 7878.95
UA5S316333.78 14516.74 12824.42 10818.81
UA5S413254.81 9655.90 11115.53 7747.17
UA5S52364.24 2345.79 1934.93 1837.42
UA5S6744.06 137.62 604.80 147.39

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Figure 1. (a) Geographical location map of the study area; (b) 3D sample plot topographic map; (c) Sample plot contour map. (b,c) use the same color scale.
Figure 1. (a) Geographical location map of the study area; (b) 3D sample plot topographic map; (c) Sample plot contour map. (b,c) use the same color scale.
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Figure 2. Quantity diagram of microtopographic samples.
Figure 2. Quantity diagram of microtopographic samples.
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Figure 3. (a) Microtopographic distribution map, color scale 1–54 represents microtopography type 1–54; (b) Slope classification distribution map, 1 represents the flat slope, 2 represents the gentle slope, 3 represents the slope, 4 represents the steep slope, 5 represents the sharp-steep slope, 6 represents the sharp slope, 7 represents the dangerous slope; (c) Slope aspect classification distribution map, 1 representative the sunny slope, 2 is representative of the semi-sunny slope, 3 represents the flat land, 4 represents the semi-shade slope, 5 represents the shady slope.
Figure 3. (a) Microtopographic distribution map, color scale 1–54 represents microtopography type 1–54; (b) Slope classification distribution map, 1 represents the flat slope, 2 represents the gentle slope, 3 represents the slope, 4 represents the steep slope, 5 represents the sharp-steep slope, 6 represents the sharp slope, 7 represents the dangerous slope; (c) Slope aspect classification distribution map, 1 representative the sunny slope, 2 is representative of the semi-sunny slope, 3 represents the flat land, 4 represents the semi-shade slope, 5 represents the shady slope.
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Figure 4. (a) Number variation diagram of tree species with different mycorrhizal types in different microtopography types from 2013 to 2018. (b) DBH sum variation diagram of tree species with different mycorrhizal types in different microtopography types from 2013 to 2018. (c) Mean DBH variation diagram of tree species with different mycorrhizal types in different microtopography types from 2013 to 2018. AM represents tree species with arbuscular mycorrhizal type. EcM represents tree species with ectomycorrhiza type. ErM represents tree species with ericoidmycorrhiza type.
Figure 4. (a) Number variation diagram of tree species with different mycorrhizal types in different microtopography types from 2013 to 2018. (b) DBH sum variation diagram of tree species with different mycorrhizal types in different microtopography types from 2013 to 2018. (c) Mean DBH variation diagram of tree species with different mycorrhizal types in different microtopography types from 2013 to 2018. AM represents tree species with arbuscular mycorrhizal type. EcM represents tree species with ectomycorrhiza type. ErM represents tree species with ericoidmycorrhiza type.
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Figure 5. Changes of quantity (left) and mean DBH (middle) of tree species with different mycorrhizal types.
Figure 5. Changes of quantity (left) and mean DBH (middle) of tree species with different mycorrhizal types.
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Figure 6. Dynamic distribution diagram of the quantity of tree species of different mycorrhizal types. 2013: trees in 2013; Dead: died trees between 2013 and 2018; Alive: alive trees from 2013 to 2018; New: new trees from 2013 to 2018; 2018: trees in 2018; AM: AM type tree species; EcM: EcM type tree species; ErM: ErM type tree species.
Figure 6. Dynamic distribution diagram of the quantity of tree species of different mycorrhizal types. 2013: trees in 2013; Dead: died trees between 2013 and 2018; Alive: alive trees from 2013 to 2018; New: new trees from 2013 to 2018; 2018: trees in 2018; AM: AM type tree species; EcM: EcM type tree species; ErM: ErM type tree species.
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Figure 7. Correlation between topography and the quantity of tree species with different mycorrhizal types(A); Correlation between DBH changes of tree species with different mycorrhizal types and topography(B); Changes in the quantity of AM type tree species (a); Changes in the quantity of EcM type tree species (b); Changes in the quantity of ErM type tree species (c); DBH sum changes of AM type tree species (d); DBH sum changes of EcM type tree species (e); DBH sum changes of ErM type tree species (f). * indicated significant correlation at p < 0.05 level. ** indicated significant correlation at p < 0.01 level.
Figure 7. Correlation between topography and the quantity of tree species with different mycorrhizal types(A); Correlation between DBH changes of tree species with different mycorrhizal types and topography(B); Changes in the quantity of AM type tree species (a); Changes in the quantity of EcM type tree species (b); Changes in the quantity of ErM type tree species (c); DBH sum changes of AM type tree species (d); DBH sum changes of EcM type tree species (e); DBH sum changes of ErM type tree species (f). * indicated significant correlation at p < 0.05 level. ** indicated significant correlation at p < 0.01 level.
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Diao, Y.; Zhang, S.; Liu, Y.; Jin, G.; Tian, S.; Liu, Y. Effects of Topography on Radial Growth of Tree Species with Different Mycorrhizal Types. Forests 2023, 14, 546. https://doi.org/10.3390/f14030546

AMA Style

Diao Y, Zhang S, Liu Y, Jin G, Tian S, Liu Y. Effects of Topography on Radial Growth of Tree Species with Different Mycorrhizal Types. Forests. 2023; 14(3):546. https://doi.org/10.3390/f14030546

Chicago/Turabian Style

Diao, Yunfei, Su Zhang, Yulong Liu, Guangze Jin, Songyan Tian, and Yankun Liu. 2023. "Effects of Topography on Radial Growth of Tree Species with Different Mycorrhizal Types" Forests 14, no. 3: 546. https://doi.org/10.3390/f14030546

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