**4. Development History of Nepalese Alder**

The whole development history can be roughly summarized into three periods: the initial development (before 2001), the fast development (2002–2015), and the high-quality development (2016–2022) (Figure 4). Among them, the number of papers published in the early period was small, with a total of only 30 papers, and the research topics mainly focused on the growth habit and forest community structure of Nepalese alder (Figure 5a). For example, the Yunnan Institute of Forestry [19] reported its growth characteristics and corresponding habit, which is a relatively systematic study of Nepalese alder in China in this stage. Guo et al. (1999) found that the alder tree layer exerted a significant effect on precipitation interception in the central Yunnan plateau [20]. In 2002, research development entered into an accelerated period, during which the number of publications increased significantly and reached a peak in 2015 (39 articles), which was about 10 times that of 2005 (the least number of articles published in this period). This might be related to the national policy to fully launch the project of returning farmland to forest in 2002, as well as the implementation of related projects which greatly promoted the research on the fast-growing alder tree species. The focus at this stage gradually shifted to vegetation restoration and seedling growth (Figure 5b). For example, Yang et al. (2004) found that the community coverage and species composition were relatively stable in phosphate mining areas [21], so it had important application value in the restoration of natural vegetation in phosphate mining wasteland. Zhou et al. (2012) found that the presence of this species significantly increased the available nitrogen and potassium content in the soil, promoted the formation of soil agglomerate structure, and effectively accelerated the restoration process of vegetation in phosphate collection areas [22]. After 2015, the number of publications showed a downward trend, which might be related to the fact that the research has focused more on practical applications. This stage focused on soil nutrients and vegetation restoration, and related research gradually shifted to practical applications (Figure 5c); for example, the Yuanyang Rice Terraces had become a research hotspot [23,24].

**Figure 4.** Changes in the number of publications of Nepalese alder since 1981.

**Figure 5.** Keywords network map for Nepalese alder in different development stages. (**a**) Initial development, (**b**) fast development, (**c**) high-quality development.

### **5. Growth Limiting Factors and Sustainable Utilization of Nepalese Alder**

### *5.1. Growth Limiting Factors of Nepalese Alder*

The evident northern boundary and upper limit of Nepalese alder suggested that the thermal condition should be the dominant limiting factor. Noshiro et al. studied the effects of tree height, diameter at breast height, and altitude on the anatomical characteristics of Nepalese alder wood in the eastern Himalayas and found that the pore diameter, vessel length, and fiber pipe length of wood were negatively correlated with altitude, indicating that temperature was the main factor affecting its anatomical structure [25]. However, further research by Noshiro et al. suggested that at altitudes above 1800 m, the vessel and fiber lengths of Nepalese alder exhibited a decreasing trend with altitude that may be related to moisture constraints [15]. Quantifying the relative contributions of different hydrothermal factors to its growth and distribution will help to understand the biogeographic distribution pattern of this species; moreover, the selection of suitable ecological sources for plantation can provide important genetic resources reserved for mountain vegetation restoration.

In addition to hydrothermal factors, nitrogen and phosphorus are also important factors affecting the growth of Nepalese alder. Simulated nitrogen deposition experiments showed that the nitrogen addition at lower levels significantly promoted the growth of alder seedlings, whereas that at higher levels inhibited seedling biomass and reduced the investment to allocation of photosynthetic organs [13]. Phosphorus deficiency also decreased chlorophyll content in Nepalese alder seedlings [14]. In addition, environmental factors could indirectly influence the growth of Nepalese alder by affecting the activity or diversity of Frankia. For example, Jha et al. found that phosphate fertilizer treatment reduced mycorrhizal infection in alder seedlings, but it significantly stimulated the nodulation of alder seedlings [26]. It can be seen that phosphorus plays a very important role in the growth of Nepalese alder itself and Frankia, especially in humid tropical and subtropical areas where forest growth is largely affected by phosphorus restriction [27]. In all, the influence of climate, soil, and other factors on the growth and distribution of Nepalese alder should be comprehensively considered in the future.

### *5.2. Physio–Ecological Characteristics and Ecological Functions of Nepalese Alder*

As a pioneer species, Nepalese alder often occupies barren hillsides due to their strong adaptability, rapid growth, and strong tolerance to barren soil, and the nitrogen fixation effect of the symbiotic root with Frankia improves soil chemical status to a certain extent. Therefore, by improving the growth environment, Nepalese alder further promotes the growth and development of other plants. At present, most scholars have discussed the physiological and ecological characteristics of Nepalese alder (Figure 6). For example, some studies have explored the growth characteristics of the Nepalese alder and cardamom agroforestry system [11], and the productivity of mixed Nepalese alder and tea plants in gardens [9]. In addition, studies have also found that chemicals in Nepalese alder might affect the growth and development of other plants through allelopathy [28]. The study of Frankia has been a major focus of alder-related research (Figure 6). At this stage, most research has focused on genetic diversity. Studies have shown that Frankia are rich in genetic diversity, which is influenced by various factors such as climate, topography, and altitude. Through the study of the diversity of Frankia, it not only helps people to understand the origin and evolution process of Frankia, so as to build an efficient symbiotic system with strong nitrogen fixation ability and stress resistance, but also provides a scientific basis for revealing the mechanisms of the nitrogen fixation and soil improvement [29].

### 5.2.1. Soil Improvement

The roots of Nepalese alder attached with Frankia generally form symbiosis nodulation with nitrogen fixation functions [6], thereby changing the soil physicochemical properties and increasing the soil organic matter and nitrogen and phosphorus content (Figure 6). Mishra et al. (2018) analyzed the soil fertility in different forests in the eastern Himalayas, and found that the soil organic matter content of Nepalese alder forests was significantly

higher than that of other forest types, and the presence of Nepalese alder accelerated soil nutrient cycling [8]. Other studies also found that the soil total nitrogen and phosphorus, alkali-hydrolyzed nitrogen, available phosphorus, and soil microbial biomass in Nepalese alder forests were significantly higher than in other vegetation types (e.g., forests dominated by *Pseudognaphalium affine*, *Cunninghamia lanceolata*, *Michelia oblonga*, *Parkia roxburghii*, and *Pinus kesiya*) in the Yuanyang Terraces of Yunnan Province [30] and the hilly ecosystems of Northeast India [31]. Studies have also pointed out that Frankia in the roots of Nepalese alder can not only improve soil physical–chemical properties and increase soil-nutrient content, but also facilitate the reproduction of soil microorganisms and improve the activity of soil enzymes [9]. Li et al. further found that the presence of Nepalese alder increased the number of soil nitrogen-fixing bacteria in seven forest communities (*Clerodendrum bangei*, *Cunninghamia lanceolata*, *Camellia sinensis*+*Alnus nepalensis*, *Alnus nepalensis*, *Gnaphalium affine*, *Choerospondias axillaris,* and *Neolitzea chui+Schima superba*) in Yuanyang Terrace [32]. Among six different vegetation types in Yuanyang terraces, it was also found that Nepalese alder significantly increased the activity of soil proteases [30].

**Figure 6.** A framework for physio-ecological characteristics and ecological functions of Nepalese alder.

5.2.2. Effect of Nepalese Alder on Other Plants

The presence of Nepalese alder can improve soil physical and chemical properties, which in turn promotes the growth of surrounding plants (Figure 6). For example, Mortimer et al. transplanted Nepalese alder to tea (*Camellia sinensis* var. *assamica*) garden, and found that the existence of Nepalese alder increased the variety and number of fungi and bacteria in the soil, which in turn improved the productivity of tea [9]. Sharma et al. found that Nepalese alder significantly increased the soil nitrogen content in the mixed agroforestry system, thereby improving the productivity and energy conversion efficiency of cardamom communities [10]. In addition, the allelopathy of Nepalese alder can also exert a positive or negative impact on the growth of other plants to some extent. Wang et al. studied the effect of fresh leaf aqueous extract of Nepalese alder on the growth of Yunnan pine seedlings and found that the lower concentration of aqueous extract (<5 g/L) can promote the growth of seedlings, enhance root vitality, and increase chlorophyll content [28]. However, a higher concentration above 5 g/L will inhibit the growth of seedlings. Wang et al. further treated the seeds of *P. Yunnanesis* with different concentrations of extracts (800, 400, 150 mg/kg) from different organs of Nepalese alder, and found that the high concentration extracts

significantly inhibited the germination and seedling growth of *P. yunnanensis* [33]. Besides, this inhibition was weakened with the decrease of extract concentration, and eventually turned into a promoting effect. In summary, the effect of Nepalese alder on the growth of other plants is mainly manifested as a promoting effect, while the allelopathy on other plants is a bit more complicated. Generally speaking, a lower concentration of aqueous extract yields a promotion effect, and a higher one may lead to inhibition. That is, when the allelopathic intensity of Nepalese alder itself is high, it will have a negative impact on the growth of other plants, which may explain why Nepalese alder forms a pure forest in the juvenile stage with few other coexisting tree species.

### 5.2.3. Frankia Infection

Frankia infection is the most representative physiological and ecological characteristic of Nepalese alder, and Frankia can form nitrogen-fixing nodules in symbiosis with Nepalese alder roots, which improves the soil conditions in the alder forest to a certain extent (Figure 6). At present, research on Frankia with Nepalese alder has focused on its genetic diversity, nutrient absorption, and morphological variation. Among them, the genetic diversity of Frankia has attracted a lot of attention. Studies have shown that the genetic diversity of Frankia nodules is influenced by a variety of factors, including topography, climate, and altitude [29]. On one hand, Frankia is widely distributed in multiple species, indicating that it can survive in diverse habitats [34]. On the other hand, in different habitats, especially at high altitudes where the environment is harsh, environmental factors such as stronger ultraviolet radiation and drought may cause genetic instability, resulting in more replication errors and higher genetic diversity to meet survival needs [35,36]. Xiong et al. studied the genetic diversity of Frankia in five regions of Yunnan, and found that the distribution and genetic structure of Frankia were closely related to the environment, and there were dominant genotypes in different regions [37]. Tang et al. used rep-PCR to study the genetic diversity of Frankia in Nepalese alder nodules under different habitats in Yunnan, and found the genetic diversity was positively correlated with the degree of environmental stress [29]. Similarly, Dai et al. [34] found that the genetic diversity of the Frankia strain in samples of Nepalese alder nodules in the Hengduan Mountains is related to climate and glacial history. In addition to topographical and climatic factors, altitude is also an important factor affecting the genetic diversity of Frankia, and it is assumed that the greater the altitude gradient, the richer the genetic diversity of Frankia [38,39].

### **6. Perspectives**

Although there exist uncertainties about the geographical origin of *Alnus* and the role of climatic factors in shaping its distribution, the above statement indicates that low temperature should be one of the key limiting factors for its distribution. Therefore, in the context of future climate change, Nepalese alder is assumed to dominate in higher latitudes and/or altitudes, which is consistent with the hypothesis that the distribution range of Nepalese alder will expand significantly under the background of climate change, as proposed by Ranjitkar et al. [40]. Based on the maximum entropy model and related climate, soil, and topographic data, the future distribution trend of Nepalese alder under different scenarios can be further simulated.

In addition to the influence of climatic factors, the loss of phosphorus will have an impact on the coupling of Nepalese alder and Frankia to a certain extent [26]. However, there are relatively few studies concentrated on the impact of multi-environmental factors on the growth of Nepalese alder at this stage, which limits our in-depth understanding of the change trend and distribution range of Nepalese alder in future situations. In addition, the Himalayan mountains are very young and still in an active stage. Affected by geology, topography, and climatic factors, as well as the uplift of the Himalayas, the mountains are prone to geological disasters such as landslides and debris flows, which have recently caused a series of ecological and environmental problems such as forest degradation and species habitat destruction [41,42]. Therefore, strengthening the study of environmental

impacts on the growth of Nepalese alder is of great necessity to make full use of Nepalese alder which may improve soil chemical and physical status in early succession, and to accelerate the positive evolution of ecosystem functions.

Previous studies have mentioned the effects of temperature and precipitation on the anatomical structure (i.e., stem traits) of Nepalese alder. Whereas, there is still a lack of research on plant functional traits, especially root and leaf traits, which limits our understanding of the response of Nepalese alder to the changes of hydrothermal factors from different sources. In particular, this species is mainly distributed in tropical and subtropical regions, and the phenomenon of leaf feeding by insects is obvious, and the analysis of leaf morphology and related traits is significant for understanding the plant– insect interaction and its mechanism in light of climate change. This work needs to be carried out urgently.

At this stage, most of the research on Frankia focused on its genetic diversity, especially the environmental impacts (terrain, climate, and altitude) on the genetic diversity, while research on the growth and reproduction of Frankia itself has rarely been reported. Relevant research is important to explore the interconnection between Frankia and Nepalese alder, and to reveal the mechanism affecting the distribution and growth of Nepalese alder. The relationship between Frankia and alder is the key factor in using Nepalese alder for ecological restoration, and it has important theoretical and practical significance for practicing General Secretary Xi Jinping's thesis that lucid waters and lush mountains are golden mountains, and the secret to establishing an ecological civilization highland on the Qinghai-Tibet Plateau.

**Author Contributions:** Conceptualization, L.Z. and C.X.; methodology, L.Z. and C.X.; software, C.X. and W.Z.; validation, L.Z.; formal analysis, C.X.; investigation, L.Z. and C.X.; resources, L.Z.; data curation, C.X. and W.Z.; writing—original draft preparation, C.X.; writing—review and editing, C.X., L.Z., J.W., J.S. and G.C.; visualization, L.Z.; supervision, L.Z.; project administration, L.Z.; funding acquisition, L.Z. All authors have read and agreed to the published version of the manuscript.

**Funding:** The Second Tibetan Plateau Scientific Expedition and Research (STEP) Program (2019QZKK0301-1) and the Key technology research and development projects in Xizang Autonomous Regions (XZ202101ZY0005G) provided financial support.

**Institutional Review Board Statement:** Not applicable.

**Data Availability Statement:** All data used in the manuscript are already publicly accessible, and we provided the download address in the manuscript.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


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**Huawei Hu 1,2, Yanqiang Wei 2,\*, Wenying Wang 3,\* and Chunya Wang 4,5**


**Abstract:** The Qinghai–Tibetan Plateau (QTP) with high altitude and low temperature is one of the most sensitive areas to climate change and has recently experienced continuous warming. The species distribution on the QTP has undergone significant changes especially an upward shift with global warming in the past decades. In this study, two dominant trees (*Picea crassifolia* Kom and *Sabina przewalskii* Kom) and one dominant shrub (*Potentilla parvifolia* Fisch) were selected and their potential distributions using the MaxEnt model during three periods (current, the 2050s and the 2070s) were predicted. The predictions were based on four shared socio-economic pathway (SSPs) scenarios, namely, SSP2.6, SSP4.5, SSP7.0, SSP8.5. The predicted current potential distribution of three species was basically located in the northeastern of QTP, and the distribution of three species was most impacted by aspect, elevation, temperature seasonality, annual precipitation, precipitation of driest month, Subsoil CEC (clay), Subsoil bulk density and Subsoil CEC (soil). There were significant differences in the potential distribution of three species under four climate scenarios in the 2050s and 2070s including expanding, shifting, and shrinking. The total suitable habitat for *Picea crassifolia* shrank under SSP2.6, SSP4.5, SSP7.0 and enlarged under SSP8.5 in the 2070s. On the contrary, the total suitable habitat for *Sabina przewalskii* enlarged under SSP2.6, SSP4.5, SSP7.0 and shrank under SSP8.5 in the 2070s. The total suitable habitat for *Potentilla parvifolia* continued to increase with SSP2.6 to SSP8.5 in the 2070s. The average elevation in potentially suitable habitat for *Potentilla parvifolia* all increased except under SSP8.5 in the 2050s. Our study provides an important reference for the conservation of *Picea crassifolia*, *Sabina przewalskii*, *Potentilla parvifolia* and other dominant plant species on the QTP under future climate change.

**Keywords:** climate change; potential distribution; MaxEnt model; suitable habitat; average elevation
