Does Shrub Encroachment Indicate Ecosystem Degradation? A Perspective Based on the Spatial Patterns of Woody Plants in a Temperate Savanna-Like Ecosystem of Inner Mongolia, China

Round 1

Reviewer 1 Report

Dear Authors

I am sorry to tell you that I am not enthusiastic with your results and conclusions as I could not find any aspect that is not rather obvious; for me the only important messages are, that Ulmus pumila could germinate in the shrub layer and that after it is grown to the medium size it could outcompete the shrubs. So to my understanding that would mean, that the shrub encroachment in your study area would not be a main reason for a decrease of Ulmus pumila. As you did not study or mention the possible changing of the proportion of grassland (what the title is in my opinion suggesting) you should focus on that message in the conclusions. I would recommend to use your data set for a study of the soil moisture under the different layer types that were in the focus of your work. As Ulmus pumila is a phreatophyte, it would be interesting to check if there is any hydraulic lift effect. That is not very presumable by your findings but would be an interesting fact. Also I would recommend to check the age of the old Ulmus trees and to compare it with the climate situations at their seedling time.

Author Response

Responses to comments for revision of manuscript (forests-975374)

(reviewer 1)

Comment 1：I am sorry to tell you that I am not enthusiastic with your results and conclusions as I could not find any aspect that is not rather obvious; for me the only important messages are, that Ulmus pumila could germinate in the shrub layer and that after it is grown to the medium size it could outcompete the shrubs. So to my understanding that would mean, that the shrub encroachment in your study area would not be a main reason for a decrease of Ulmus pumila. As you did not study or mention the possible changing of the proportion of grassland (what the title is in my opinion suggesting) you should focus on that message in the conclusions. I would recommend to use your data set for a study of the soil moisture under the different layer types that were in the focus of your work. As Ulmus pumila is a phreatophyte, it would be interesting to check if there is any hydraulic lift effect. That is not very presumable by your findings but would be an interesting fact. Also I would recommend to check the age of the old Ulmus trees and to compare it with the climate situations at their seedling time.

Response:

 First of all, we thank for your valuable advices, and most of the suggestions are very important for my future scientific research.

But in this paper, we focused on the spatial pattern distribution of shrubs and trees by establishing large sample plots following the plot standards of the Center for Tropical Forest Science (CTFS) network in the temperate savanna-like ecosystem of Inner Mongolia, China, which has been destroyed but received less attention.

There recently were some studies that combined traditional spatial patterns and tree growth, as well as their relations with environmental factors (such as soil moisture, temperature) just as you suggested. For example, the paper is :

Sigdel S R , Liang E , Wang Y , et al. Tree‐to‐tree interactions slow down Himalayan treeline shifts as inferred from tree spatial patterns[J]. Journal of Biogeography. https://doi.org/10.1111/jbi.13840

However, in this manuscript, we try to fucus on the spatial patterns and its ecological implication. But in future, we will do more research to find the environment condition changes after shrub encroachment.

Reviewer 2 Report

This is an interesting study about the temperate savanna vegetation in Inner Mongolia, but it contains some flaws that have to be clarified during the revision. Hope the authors are willing to address my comments below.

Introduction:

As the authors mention in Introduction, shrub encroachment may indicate both degradation and regeneration. I think that this role is strongly depends on different factors, such as the type of ecosystem, past management practices, the current level of biodiversity, climate change, etc. So, I think that the Introduction should be complement with a longer paragraph in which the authors bring examples about the potential effects of shrub encroachment in different ecosystems (both positive and negative examples). I strongly recommend reading and citing the following papers, and other relevant papers:

 

Tölgyesi C, Bátori Z, Gallé R, Urák I, Hartel T (2018)

Shrub encroachment under the trees diversifies the herb layer in a Romanian silvopastoral system

Rangeland Ecology & Management 71, 571-577

 

Erdős L, Cserhalmi D, Bátori Z, Kiss T, Morschhauser T, Benyhe B, Dénes A

Shrub encroachment in a wooded-steppe mosaic: combining GIS methods with landscape historical analysis. Applied Ecology and Environmental Research 11, 371-384

 

lines 87-90: These sentences should be moved to the Material and Methods

 

Figure 1: Map scale is absent

 

lines 119-121: Sampling design in not clear in its current form. It would be great to see a schematic figure about the sampling plot. What does ‘dynamic plot’ mean? Do the authors think that 1 sampling plot can be representative enough to describe and analyse this ecosystem? I think this is a limiting factor for the interpretation of results.

 

lines 127-133: In my opinion, the description of the methodology (data analysis) is not clear in its current form. I suggest sharing more information about this statistical method. For instance, the authors use the term ‘toroidal shift’ and ‘antecedent condition’ null models in the legend of Figure 3 (lines 176-177), but these terms have not been mentioned in the method section (data analysis). It is also true for Figure 5, where the authors use the term ‘independent null model’.

 

Table 1: I do not understand why Ribes diacanthum (Grossulariaceae) and Caragana microphylla Lam. (Fabaceae) are in the same row of the Table (‘Shrubs-Ribes diacanthum’ is mentioned in the Species column). Sometimes the name of author (e.g., Lam.) has been added after the scientific name of a species, but sometimes it is absent. I suggest consistently using the name of species throughout the manuscript.

 

lines 141-144: Please use italics when you mention the scientific names of species.   

 

lines 147-149: The authors mention the heights of trees in this paragraph, but they did not mention in the methods that they measured this parameter of trees.

 

lines 153-158: You did not mention in the materials and methods section that you recorded the herbs and estimated their cover on the field.  

 

The order of Figure 2 and Figure 3 is incorrect.

 

I suggest using the terms ‘positive relationship’ and ‘negative relationship’ instead of ‘negative correlation’ and ‘positive correlation’ throughout the MS.

 

Figures 2-7: I think that the authors did not use the correct values for scales in all cases. For instance, they mention that ‘juvenile trees (DBH < 5 cm) were significantly aggregated at the 0-12 m scale’ (lines 164-165), but the figure does not show that. I suggest revising all figures and adding the correct values for scales.

 

lines 171-174: These are not results, rather a discussion.

 

Figure 5: Ribes diacanthum instead of ribes diacanthum, Salix linearistipularis instead of Salix linearitipularis (see also Figure 7)

 

line 211: Salix myrtilloides instead of Salix gordejevii? (see Figure 7)

 

Figure 6: please do not use italics in the case of var. (species: Salix microstachya var. bordensis)

 

Figure 7: please use spaces before and after the abbreviation vs.

 

line 228: It is surprising for me that the authors use this title for this subsection, because they did not measure and analyse soil moisture

 

line 275: I suggest deleting the following part of the sentence: ‘this phenomenon is called shrub encroachment.’, because it contains well-known and therefore redundant information for ecologists.

 

Lines 282-287: You provide possible explanations for the results showed by this study. However, after that you clearly state that this study demonstrated that shrub encroachment has disrupted the normal succession pattern in the U. pumila community. It would be great to see more explanations for this statement.

Author Response

Responses to comments for revision of manuscript (forests-975374)

(reviewer 2)

 

Comment 1. Introduction: As the authors mention in Introduction, shrub encroachment may indicate both degradation and regeneration. I think that this role is strongly depends on different factors, such as the type of ecosystem, past management practices, the current level of biodiversity, climate change, etc. So, I think that the Introduction should be complement with a longer paragraph in which the authors bring examples about the potential effects of shrub encroachment in different ecosystems (both positive and negative examples). I strongly recommend reading and citing the following papers, and other relevant papers:

• Tölgyesi C, Bátori Z, Gallé R, Urák I, Hartel T (2018) Shrub encroachment under the trees diversifies the herb layer in a Romanian silvopastoral system. Rangeland Ecology & Management 71, 571-577
• Erdős L, Cserhalmi D, Bátori Z, Kiss T, Morschhauser T, Benyhe B, Dénes A. Shrub encroachment in a wooded-steppe mosaic: combining GIS methods with landscape historical analysis. Applied Ecology and Environmental Research 11, 371-384

Response: Many thanks for your suggestions. We accepted the reviewer's suggestion to add these additional information (See lines 51-69). The relevant papers had been added in the manuscript as follows: (See lines 402-407)

Shrub encroachment in grasslands and the densification of woody plant cover in savannas have been widely documented across many arid and semiarid areas of the world [1-4], including in South America, Australia, and the warm deserts of the southwestern United States. However, until now, there has been a clear division of opinion about its ecological indication. One view is that shrub encroachment is an indicator of land degradation that is often associated with ecosystem degradation [5]: such as declines in forage productivity, biodiversity, and socioeconomic potential, as well as increased erosion [6]. However, an alternative viewpoint proposing that shrub emergence is a sign of the restoration of degraded ecosystems has emerged recently [7, 8], considered to support the biodiversity and a variety of ecosystem service [9]. In addition, shrub encroachment has been described as an alternative stable state occurring several times during the last two millennia in African savannas [10]. Some research also found that the role of shrub species was important in the rehabilitation of degraded sandy land ecosystems [11]. Furthermore, different opinions exist as to the causes of shrub encroachment in different type of ecosystem [12], some research found that underuse leads to shrub and subsequent tree encroachment, and finally conversion to forest [12], however, overgrazing usually caused shrub encroachment in Africa and Mongolia Plateau [10]. This difference in the perception of shrub encroachment could lead to completely different judgments of the states and transitions of shrub-encroached ecosystems, which would further affect decisions about their conservation and management [13]. An innovative study [14], combined with the landscape history and other environmental factors, thus quantifies the process and indicative significance of shrub encroachment, and provided us with new ideas. In order to the indicative significance of shrub encroachment, this mainly depends on different factors, such as the type of ecosystem, past management practices, the current level of biodiversity, climate change, etc. Therefore, more attention needs to be paid to ecosystem changes after shrub encroachment to clarify their ecological significance, especially the significance of the degree of shrub encroachment and changes in distribution patterns and structure. This information could then be used to quantify the ecological indications of shrub encroachment.

 

Comment 2. lines 87-90: These sentences should be moved to the Material and Methods.

Response: Thank you for your suggestion. These sentences have been moved to the Material and Methods as shown in lines197~102.

 

Comment 3. Figure 1: Map scale is absent

Response: corrected (as Figure 1)

 

Comment 4. lines 119-121: Sampling design in not clear in its current form. It would be great to see a schematic figure about the sampling plot.

Response: Thank you for your suggestion. A schematic figure about the sampling plot was added in Figure 1.

 

Comment 5. What does ‘dynamic plot’ mean?

Do the authors think that 1 sampling plot can be representative enough to describe and analyse this ecosystem? I think this is a limiting factor for the interpretation of results.

Response: Thank you for your suggestion.

In the part of method, we mainly refer to the construction of large sample plot. The Center for Tropical Forest Science (CTFS) – Forest Global Earth Observatory (ForestGEO) is a global network of forest research sites that is strategically poised for monitoring, understanding, and predicting forest responses to global change. This international partnership currently includes 59 long-term forest dynamics research sites in 24 countries, which have been monitored continuously since as early as 1981 (Barro Colorado Island; Condit, 1995). The network applies a unique standardized tree census protocol across all of the world’s major forest biomes, allowing comparison across sites (e.g., Condit, 2000; Muller-Landau et al., 2006a,b; Chave et al., 2008; Chisholmet al., 2013, 2014).

Therefore, one of the main work of my paper is to explore the spatial pattern distribution of shrubs and trees by establishing large sample plots following the plot standards of the Center for Tropical Forest Science (CTFS) network in the temperate savanna-like ecosystem of Inner Mongolia, China, which has been destroyed, received less attention but have great significance.

We think that a large sample plot can basically represent the problem we want to study, but your suggestion is also very important, so we modify the description of the sample plot and supplement the method of investigation. At the same time, in order to avoid some misleading words. We accepted the reviewer's suggestion to change word "dynamic plot " into word "sample plot" in all the paper. (See lines 127~147)

Most work about the spatial distribution and interaction of woody plants had been done in single hectare or smaller plots, but the relative rarity of many species in forests necessitated large-scale census plots. Thus the plot usually with more than 5 hectares, named as large plot is considered as the representative of local vegetation，which could cover the local typical vegetation and topography in a region. By a large plot, the interference of scale and environmental heterogeneity could be avoided for the study on vegetation composition, pattern and biodiversity [41]. This method by a large plot instead of many normal-size plots has been widely used in global forest dynamic monitoring.

In this study, this large plot method was applied and one large plot with the area of 25 ha (500 m × 500 m) was established following the plot standards of the Center for Tropical Forest Science (CTFS) network [41]. It located in in the Otindag Sandy Land in Inner Mongolia, China (115°16'E, 42°50'N), in a typical area of Ulmus pumila-dominated temperate savanna-like ecosystem (Fig. 1). 

Then, this large plot was further divided into 625 subplots (20 × 20 m). All free-standing trees with stem diameters at breast height (DBHs) of more than one centimeter and all shrubs were tagged, mapped and identified to species during the summer of 2013-2014. The coordinates of woody plants in each subplot were recorded using an Electronic Total Station with the southwestern corner of the subplot as the origin. Additionally, in the center of each subplot, a small plot with the size of 1 m × 1 m was setup. Then, it’s all herbaceous species were identified and their cover ratios and numbers were recorded.

All U. pumila trees were classified into three categories according to their DBH [42], namely, old trees (DBH ≥ 20 cm), medium trees (5 cm ≤ DBH < 20 cm), and juvenile trees (DBH < 5 cm) (Table 1).

 

• Figure 1. Map of the Otindag Sandy Land and the location of the study region(a: location; b:sample map; c and d: pictures of the temperate savanna-like ecosystem; e: contour map of sample plot, unit/m).

 

 

Fig.  Contour map (left unit/m) and perspective diagram (right) of the plot

 

Comment 6. lines 127-133: In my opinion, the description of the methodology (data analysis) is not clear in its current form. I suggest sharing more information about this statistical method. For instance, the authors use the term ‘toroidal shift’ and ‘antecedent condition’ null models in the legend of Figure 3 (lines 176-177), but these terms have not been mentioned in the method section (data analysis). It is also true for Figure 5, where the authors use the term ‘independent null model’.

Response: Thank you for your suggestion. We modified this part as following (see lines 149-169):

2.3. Data analysis

The pair-correlation function g(r) is a statistical method used to estimate the number of points within concentric rings at a distance r rather than within a certain radius and is especially sensitive to small-scale effects [43, 44]. There are two g(r)function, i.e, univariate and bivariate g(r), in this study, the univariate g (r) function was used to analyze the spatial distribution patterns within of woody plants, and the bivariate g (r) function to quantify the both intra- and interspecific spatial association among tree and shrub plants [43, 44].

Firstly, the univariate g(r) function was used to analyses three tree categories (old trees, medium trees and juvenile trees), and for all shrub spieces. The null model of complete spatial randomness(CSR) as a null hypothesis was used all the univariate analyses. Secondly, for the bivariate analyses, two cases were considered. One case was that the relationship between small and large trees was considered. Since large trees may impact the distribution pattern of small trees within their area of influence (competition), a bivariate g function analysis was conducted for these two size classes using both the toroidal shift and the antecedent condition null model options [43]. This tests whether the patterns of distribution of small and large trees were generated by independent processes. The antecedent condition model tests whether one pattern (small trees) is influenced by a second pattern (large trees), assessing whether there are more (or fewer) small trees in the neighborhood of large trees than expected under a random distribution of small trees [43]. The second case concerns the interaction between trees and shrubs. Because the spatial distributions of plants in plots seem to be affected significantly by drought stress and habitat heterogeneity (e.g., soil patch and microtopography), we examined the spatial association between the two species with the independent null model [44].

 

 

Comment 7.  Line 48. Comma (,) should be a period (.)

Response: ‘corrected

 

Comment 8. lines 141-144: Please use italics when you mention the scientific names of species. 

Response: corrected (see lines 179-182)

 

Comment 9. lines 153-158: You did not mention in the materials and methods section that you recorded the herbs and estimated their cover on the field. .

Response: Thank you for your suggestion. The method on the herbs and their cover on the field had been added. (see lines 127-147)

 

Comment 10.  The order of Figure 2 and Figure 3 is incorrect. 

Response: Corrected (see lines 210~214).

 

Comment 11. I suggest using the terms ‘positive relationship’ and ‘negative relationship’ instead of ‘negative correlation’ and ‘positive correlation’ throughout the MS.

Response: Thank you. The correction has been made. This is a problem of my language.

 

Comment 12. Figures 2-7: I think that the authors did not use the correct values for scales in all cases. For instance, they mention that ‘juvenile trees (DBH < 5 cm) were significantly aggregated at the 0-12 m scale’ (lines 164-165), but the figure does not show that. I suggest revising all figures and adding the correct values for scales. 

Response: All figures have been revised and the scales have been added.

 

Comment 13. lines 171-174: These are not results, rather a discussion.

Response: These sentences have been moved to the Discussion (see lines 209)

 

Comment14. Figure 5: Ribes diacanthum instead of ribes diacanthum, Salix linearistipularis instead of Salix linearitipularis (see also Figure 7)

Response: Corrected (see Figure5,7)

 

Comment15. line 211: Salix myrtilloides instead of Salix gordejevii? (see Figure 7)

Response: Corrected (see Figure 7)

 

Comment16. Figure 6: please do not use italics in the case of var. (species: Salix microstachya var. bordensis)

Response: Corrected (see Figure6)

 

Comment17. Figure 7: please use spaces before and after the abbreviation vs.

Response: Corrected (see Figure7)

 

Comment18. line 228: It is surprising for me that the authors use this title for this subsection, because they did not measure and analyse soil moisture

Response: Thank you for your suggestion. The title of the subsection has been modified  (see lines 259-260)

4.1. Spatial patterns of U. pumila trees and their mechanism of formation in the temperate savanna-like ecosystem

Comment18. line 275: I suggest deleting the following part of the sentence: ‘this phenomenon is called shrub encroachment.’, because it contains well-known and therefore redundant information for ecologists

Response: Corrected.

 

Comment19. line 275: Lines 282-287: You provide possible explanations for the results showed by this study. However, after that you clearly state that this study demonstrated that shrub encroachment has disrupted the normal succession pattern in the U. pumila community. It would be great to see more explanations for this statement.

Response: Thank you for your suggestion. This has been modified as following (see lines 351-356):

In conclusion, shrub encroachment was observed in a temperate savanna-like ecosystem in northern China, possibly as a result of both grazing and climate change. Shrub encroachment in this area has changed composition and spatial pattern of the original tree-dominated savanna. Due to severe damage to the U. pumila-dominated temperate savanna-like ecosystem, especially for woody vegetation, ecological degradation has occurred, such as decreasing temperate savanna-like area, loss of structural integrity, poor population regeneration, and changing spatial patterns.

 

Finally, Thanks for your suggestion. These two papers are really important to my research. Through your share papers, we found that there are similar ecosystems in Europe and there are also problems that we are interested in. Such as, in China, forest resources and grasslands are managed by different national departments and implement different management policies. This makes the temperate savanna-like ecosystem very embarrassing, because it belongs to neither grassland nor forest, this defect in the national management system has caused great damage to the temperate savanna-like ecosystem in the past few decades. We are pleasantly surprised to find that there is also such a problem in your share paper (Tölgyesi C,2018). theirlong-term survival is uncertain.Wood-pastures are forced into the categories of forest or pasture by policymakers, but the multifunctional system of wood-pasture rarely exists as a legal category and therefore often remains unprotected. As a result socioeconomic trends like intensification of livestock production through tree removal or land abandonment threaten wood-pastures all over Europe (Manning et al., 2006; Bergmeier et al., 2010).A good news is that the Chinese government realized this problem two years ago and classified land, forestry and grassland as one department management.

The paper Erdős L et al., (2013) is also very useful to us. Part of the distribution of the temperate savanna-like ecosystem in China is the Mongolian living areas, they are mainly grazing, part is the Han living areas, they are mainly farming, we have want to combined with the history of land use, analyze the impact of grazing system and farming culture in different regions on the temperate savanna-like ecosystem, but it is a pity that we do not have such detailed and real historical data like the paper Erdős L et al., (2013). It's a really good way.

Reviewer 3 Report

The manuscript presents an interesting and important study and in general, I find it well done. However, there are some questions, corrections, and shortcomings for further consideration. So I have to recommend revising the manuscript according to the issues listed below.

Title

In the title, the authors applied the term “temperate savanna” for studied ecosystems. However, in the Introduction section, they call the ecosystem “savanna-like woody herbaceous complex ecosystem in association with grass” (line 58-59). Thereafter (line 60) they introduce the term “savanna” for the same ecosystem type. In general, I don’t agree with defining these ecosystems as “savanna” because traditionally it is applied to equatorial and subequatorial landscapes and recognized as a separate tropical-subtropical biome. And there are many special traits in the savanna biome which are not typical for temperate savanna-like ecosystems. From my point of view, references (32-33) at line 100 do not provide enough evidence to define those ecosystems as savanna. Moreover, authors call those ecosystems “forest-steppe ecotone” which means the other kind of biome but not a savanna. Furthermore, in section 4.1 authors compare “Ulmus pumila trees of the temperate savanna” with “Ulmus pumila trees in temperate forests” (lines 231-232); in section 4.4 “…temperate savanna, once widely distributed throughout the forest-steppe ecotone …” (lines 270-271). These sentences also look contradictory because of mixing biomes typically belonging to different climatic zones – temperate and tropical/subtropical.

In general, application the term “savanna” for those temperate ecosystems blurs the term “savanna” itself and generates the uncertainty of the term “biome”.

So I suggest modifying the title by using “in the temperate savanna-like ecosystem” (or landscape) instead of “savanna”, and the text as well as figures should be appropriately corrected.

 

Lines 62-63

Authors separated “land use change and economic development”, but it might be just a consequent event, so it looks like to say “land use change in the course of economic development” will be preferable.

Lines 102-103

The mean annual precipitation is 350 mm, so please explain how the pan evaporation reaches 1900 mm?

Lines 121-125

It is not clear if the authors accounted for Ulmus pumila trees with stem DBH less than 1 cm? Please clarify.

Line 139 (Table 1)

1) Only two species (Betula fruticosa and Caragana microphylla) have been provided with the authors for the Latin name. Please correct.

2) The name for group Shrubs-Ribes diacanthum is inconsistent; moreover, the group included 2 species from different families (Grossulariaceae and Fabaceae). To divide the group looks like a better solution.

Line 142

If authors will provide authors for the Latin names of plants in Table 1 there will be not necessary to mention authors of the Latin names in the text here (namely Betula fruticosa, Caragana microphylla) as well as further (lines 182, 184, etc.).

Line 143

Put the comma after “diacanthum”.

Lines 156-157

Can you provide the reference for “the total number of higher plants observed in the Otindag Sandy Land”?

Line 157

Add “mostly”: The herbs belonged mostly to …

Line 176

Correct Figure’s number 2 instead of 3.

Line 179

Correct Figure’s number 3 instead of 2.

Lines 248-249

“… the old U. pumila tree might be the source of the shrubs and juvenile trees”.

It seems there is a mistake because it is not understandable how the U. pumila tree might be the source of the shrubs?

Section 4.2, especially Lines 249-257

I think the impact of resting livestock is the crucial factor here since the authors claim that “bare soil circle” under old trees is formed by animals. In order to prove the significant influence of the old trees on the light sufficiency and soil moisture under the crown, the collection of special data (with light intensity as well as soil moisture measurements) in the undisturbed area is required.

Consequently, it is not possible to be agreed with the conclusion from section 4.2.

Section 4.3

The issue discussion is doubtful. The only Caragana microphylla surely can provide some fertilization of the area due to the symbiosis with Azotobacter spp. What about other shrubs, if there is some facilitation of juvenile Ulmus pumila tree survival by most shrub species? On the other side, if authors discuss the competition between groups of Ulmus pumila as far as between groups of Ulmus pumila and shrubs, so why this issue was not discussed in this section?

In general, I agree with most of the findings presented in the manuscript. However, the reasons for negative relationships between old and juvenile Ulmus pumila trees should be discussed more carefully. The same concern relates to relationships between juvenile Ulmus pumila and shrub species. The latter is especially important since the succession trajectory might be closely related to these relationships.

Author Response

Responses to comments for revision of manuscript (forests-975374)

(reviewer 3)

Comment1. Title In the title, the authors applied the term “temperate savanna” for studied ecosystems. However, in the Introduction section, they call the ecosystem “savanna-like woody herbaceous complex ecosystem in association with grass” (line 58-59). Thereafter (line 60) they introduce the term “savanna” for the same ecosystem type. In general, I don’t agree with defining these ecosystems as “savanna” because traditionally it is applied to equatorial and subequatorial landscapes and recognized as a separate tropical-subtropical biome. And there are many special traits in the savanna biome which are not typical for temperate savanna-like ecosystems. From my point of view, references (32-33) at line 100 do not provide enough evidence to define those ecosystems as savanna. Moreover, authors call those ecosystems “forest-steppe ecotone” which means the other kind of biome but not a savanna. Furthermore, in section 4.1 authors compare “Ulmus pumila trees of the temperate savanna” with “Ulmus pumila trees in temperate forests” (lines 231-232); in section 4.4 “…temperate savanna, once widely distributed throughout the forest-steppe ecotone …” (lines 270-271). These sentences also look contradictory because of mixing biomes typically belonging to different climatic zones – temperate and tropical/subtropical.

In general, application the term “savanna” for those temperate ecosystems blurs the term “savanna” itself and generates the uncertainty of the term “biome”.

So I suggest modifying the title by using “in the temperate savanna-like ecosystem” (or landscape) instead of “savanna”, and the text as well as figures should be appropriately corrected.

Response: This is a good suggestion, and also a question that has been puzzling us all the time. We accepted the reviewer’s suggestion to change the description.

 

Comment 2. Lines 62-63 Authors separated “land use change and economic development”, but it might be just a consequent event, so it looks like to say “land use change in the course of economic development” will be preferable.

Response: Changed (see line76).

 

Comment3. Lines 121-125 It is not clear if the authors accounted for Ulmus pumila trees with stem DBH less than 1 cm? Please clarify.?

1) Only two species (Betula fruticosa and Caragana microphylla) have been provided with the authors for the Latin name. Please correct.

2) The name for group Shrubs-Ribes diacanthum is inconsistent; moreover, the group included 2 species from different families (Grossulariaceae and Fabaceae). To divide the group looks like a better solution.

Response: This is a very good problem, because we use the observation method of fixed large sample plots following the plot standards of the Center for Tropical Forest Science (CTFS) network, and the work is very large in the range of 25 hectares. at first, we only measured the woody plants with DBH above 1cm according to the requirements of large sample plots, In addition, U. pumila seedlings often suffer from severe water stress during dry summers is caused by repeated cycles of drying in the upper soil layers [52]. Wang et al. [53] noted that more than 90% of the current-year seedlings in fenced plots died because of their vulnerability to drought.

But we think your suggestion is very good. In some small-scale studies (1 hectare), we have gone to observe the changes of seedlings (DBH < 1cm).

We changed the table(see lines 177-178)

 

Comment 4. L28: Line 143 Put the comma after “diacanthum”.

Response: added the information

 

Comment 5. L38: Lines 156-157 Can you provide the reference for “the total number of higher plants observed in the Otindag Sandy Land”?

Response: added the reference(see lines 195-196)

 

Comment 6. L41: Line 157 Add “mostly”: The herbs belonged mostly to …

Response: added the information (see lines 195-196)

 

Comment 7. Line 176 Correct Figure’s number 2 instead of 3.

Response: Correct Figure’s number (see lines 210-214)

 

Comment8. Lines 248-249 “… the old U. pumila tree might be the source of the shrubs and juvenile trees”. It seems there is a mistake because it is not understandable how the U. pumila tree might be the source of the shrubs?

Response:  changed the mistake.

 

Comment 9. Section 4.2, especially Lines 249-257 I think the impact of resting livestock is the crucial factor here since the authors claim that “bare soil circle” under old trees is formed by animals. In order to prove the significant influence of the old trees on the light sufficiency and soil moisture under the crown, the collection of special data (with light intensity as well as soil moisture measurements) in the undisturbed area is required.

Consequently, it is not possible to be agreed with the conclusion from section 4.2.

Response: This is a good question, and the picture can confirm your deduction. So we perfected this part of the content. (see lines 281-325)

 

(picture: The interference of livestock to old trees)

 

4.2. Spatial interactions among trees and shrubs—old U. pumila trees inhibit the survival of juvenile trees and shrubs

In this study, a negative relationship between old U. pumila trees and juvenile trees was found, and significant competition between most shrub species and old U. pumila trees was also found. From these findings, we can conclude that the environment around old U. pumila trees is not suitable for the survival of juvenile trees or shrubs[53 ,55]. This further demonstrates that seedling regeneration in U. pumila-dominated savanna-like ecosystem depends strongly on medium trees rather than on old trees. This situation is likely due to the influence of grazing. Historically, the U. pumila-dominated savanna-like ecosystem of the Otindag sand land was an important pasture source, providing a large amount of forage for livestock[51 ,56]. Although precipitation and soil moisture have been the main limiting factors affecting population regeneration of woody plants in arid and semiarid areas [57], grazing has become an important factor affecting population regeneration; long-term continuous heavy grazing has resulted in the destruction of topsoil and degradation of the rangeland [58]. In this savanna-like ecosystem, the area under the tree crown is usually occupied by resting livestock taking shelter from the summer heat and the intense ultraviolet radiation. Thus, the soil under the crown may be destroyed and become hardened due to the animals’ trampling and reclining, and a "bare soil circle" will sometimes form under these trees [59]. This is similar to the phenomenon of piospheres caused by grazing, It was found by some studies that  the soil moisture and nutrients in the piospheres are significantly lower than those in other areas, this may be the main reason for the change of vegetation composition and pattern, such as reduction in the density and production of forage, changes in the species composition of forage vegetation, shrub encroachment and so on [59]. Some research focus on the "bare soil circle" form under these trees in this savanna-like ecosystem, and also proved that the soil moisture and nutrients on the "bare soil circle" are lower than those outside the crown of elm [60]. These factors are unfavorable to the survival of any individual plant, including juvenile trees, shrubs and grasses. Therefore, the disturbance of livestock caused by overgrazing may be one of the main reasons for the competition of old U. pumila trees and juvenile trees and shrubs in this region.

In contrast, medium trees exhibited a significant positive association with juveniles at smaller scales. This suggests that the environmental conditions, such as light availability and soil moisture, around medium trees are more favorable for juvenile trees than those around adult trees. Some studies also show that the soil nutrients (organic matter, total nitrogen, available phosphorus) and soil moisture under the middle trees crown are significantly higher than those outside the crown, and there are better microenvironmental conditions (light, temperature, humidity, etc.) under the crown[60]. In addition, the disturbance of livestock to medium trees is less than that to old trees.

Different shrub species showed different spatial relationship with U. pumila in this study. We found that there was some facilitation of juvenile U. pumila tree survival by shrub species, such as C. microphylla. This may be because the emergence of shrubs improves soil moisture and nutrient conditions [62,63], and C. microphylla surely can provide some fertilization of the area due to the symbiosis with Azotobacter spp. This demonstrates that some shrubs provide some fertilization to the area in which they grow, thereby providing a favorable environment for U. pumila seedling growth. These results also showed that there were mutualistic relationships between juvenile trees and the shrubs S. gordejevii, and S. aquilegifolia, this is might because S. aquilegifolia and C. microphylla, as spiny shrubs, can provide shelter for elm seeding, such as holding back sand and reducing damage from livestock and wind, which would protect the juvenile U. pumila trees [64]. Our results were similar to those of Csaba Tölgyesi et al[9], who also found that thorny shrubs were important for supporting the biodiversity of these wooded rangelands, as well as facilitating the regeneration of trees by acting as nurse species.

 

Comment 10. Section 4.3

The issue discussion is doubtful. The only Caragana microphylla surely can provide some fertilization of the area due to the symbiosis with Azotobacter spp. What about other shrubs, if there is some facilitation of juvenile Ulmus pumila tree survival by most shrub species? On the other side, if authors discuss the competition between groups of Ulmus pumila as far as between groups of Ulmus pumila and shrubs, so why this issue was not discussed in this section?

In general, I agree with most of the findings presented in the manuscript. However, the reasons for negative relationships between old and juvenile Ulmus pumila trees should be discussed more carefully. The same concern relates to relationships between juvenile Ulmus pumila and shrub species. The latter is especially important since the succession trajectory might be closely related to these relationships.

Response: According to your opinion, we have modified the structure of this part and explained the relationship between shrubs and trees in more detail. (see lines 281-325)

Round 2

Reviewer 1 Report

dear Mrs Xu as the author did not accept any of my suggestions to improve the manuscript I am not able to change my opinion; I still miss a proof of their interpretations on the found pattern of the Ulmus pumila trees related to the shrubs and even an answer to the question of the heading is missing. with kind regards Martin Magnes

Author Response

Thanks for your valuable advices，we think your suggestion is very important and what we need to focus on in our future research. I hope to have the opportunity to achieve some of your suggestions after doing more relevant data investigation, which is really good ideas.

But the innovation of this paper is mainly through the large sample following the plot standards of the Center for Tropical Forest Science (CTFS) network, systematically explain the relationship between trees and shrubs the temperate savanna-like ecosystem.

Thanks again for your valuable advice.

Best wishs.

Reviewer 2 Report

In my opinion, this manuscript has improved substantially after the revision. Only some minor comments have remained from my side. If the Authors address these, I can recommend this paper for publication in Forests.

 

Comments:

line 49: Please remove the colon from this sentence and use comma after the citation [5]

line 52: ‘variety of ecosystem services’ instead of ‘variety of ecosystem service’

line 54: ‘Some studies also found…’ instead of ‘Some research also found…’

line 56: ‘different types of ecosystems’ instead of ’different type of ecosystem’

line 56: ‘some studies…’ instead of ‘some research’

line 58: ‘causes’ instead of ‘caused’

line 62: ‘quantified’ instead of ‘thus quantifies’

lines 63-65: I suggest rephrasing this sentence, because it is hard to read and understand in its current form.  

line 133: ‘This method has been widely used in global forest dynamic monitoring.’ instead of ’This method by a large plot instead of many normal-size plots has been widely used in global forest dynamic monitoring.’

line 137: ‘It located in the’ instead of ’It located in in the’

line 139: ’20 m × 20 m’ instead of ’20 × 20 m’

line 144:   ’All herbaceous species…’ instead of ’Then, it’s all herbaceous species…’

line 155: ’was used to analyse…’ instead of ’was used to analyses…’

line 157: ’was used for all’ instead of ’was used all’

Table 1, first row: Species

lines 179-180: Please use a space after the genus name of species, for instance: S. linearistipularis…

line 194: ‘representing’ instead of ‘this represents’

Figure 3, right part, title: U. pumila medium trees VS U. pumila juvenile trees

line 246: please use a space after the word scales

line 275: ‘during dry summers that is caused by repeated’ instead of ’during dry summers is caused by repeated…’

line 285: ‘in the U. pumila-dominated savanna-like ecosystem’ instead of ’in U. pumila-dominated savanna-like ecosystem’

line 288: Please use a space before the citations

line 296. Please use a full stop after the word grazing.

line 300: ‘Some studies…’ instead of ‘Some research…’

line 300: ‘formed’ instead of ‘form’

line 304: ‘for the negative relationships between old U. pumila’ instead of ’for the competition of old U. pumila’

line 310: ‘under the crown of medium trees’ instead of ‘under the middle trees crown’

lines 313-315 (We found…): Please rephrase this sentence for better understanding

line 320: Please use italics only in the case of species names

line 323: ’to those of Tölgyesi et al. [9],’ instead of ‘to those of Csaba Tölgyesi et al[9],’

line 324: ‘of wooded rangelands’ instead of ’of these wooded rangelands’

lines 348 and 353: ‘area has resulted in changes in the composition ‘instead of ‘area has changed composition’

lines 390-392: The correct citation is: Tölgyesi, C., Bátori, Z., Gallé, R., Urák, I., & Hartel, T. (2017) Shrub encroachment under the trees diversifies the herb layer in a Romanian silvopastoral system. Rangeland Ecology & Management 71, 571-577.

lines 405-407: The correct citation is: Erdős, L., Cserhalmi, D., Bátori, Z., Kiss, T., Morschhauser, T., Benyhe, B. & Dénes, A. (2013) Shrub encroachment in a wooded-steppe mosaic: combining GIS methods with landscape historical analysis. Applied Ecology and Environmental Research 11, 371-384.

References: Please check all references in the reference list carefully, and use the formatting (e.g. the use of italics, commas, full stops) according to the Journal.

Author Response

please see the attachment.

Author Response File: Author Response.docx