1. Introduction
The climate has been warming during the past decades, and a 0.3–4.8 °C increase in global mean annual air temperature has been projected for the 21st century [
1]. The warming has led to substantial degradation of permafrost, as evidenced by deepening active layers (the layer above permafrost which thaws in summer and refreezes in winter) and rising ground temperatures [
2,
3,
4,
5,
6]. The greatest warming of permafrost has been observed in the zones of the coldest permafrost; in the High Arctic at an average rate of 0.04 °C/yr (2007–2016) [
2], and at a rate of 0.02 °C/yr (1980–2017) in the Interior of the Qinghai-Tibet Plateau (QTP) [
7]. Meanwhile, data from field observations show a globally deepening active layer in permafrost regions [
8,
9]. In the continuous permafrost zone in the western Russian Arctic, the active layer thickness (ALT) in tundra increased at a rate of 0.62 cm/yr from 1997 to 2018 [
10], while in the central areas on the QTP, the ALT increased at a rate of 1.95 cm/yr from 1981 to 2018 [
11].
Permafrost degradation leads to vegetation changes, including changes in vegetation cover [
12], species diversity [
13], biomass [
14], and plant species composition [
15]. Vegetation changes can follow two pathways: (1) from terrestrial vegetation to aquatic vegetation coupled with forest, to sedges and mosses in lowland boreal forest underlain by ice-rich permafrost [
16]. Permafrost degradation results in the melting of ground ice and increases the supra-permafrost water table, further causing the mortality of trees and the colonization of aquatic herbaceous plants [
17]; (2) from hygrophilous to meso-xerophytic and xerophytic species [
18]. For example, in the High Arctic, moss could be replaced by herbaceous plants [
19,
20], while on the QTP, alpine meadows are shifting to alpine steppes; meanwhile, a decline in vegetation cover and diversity has been observed [
21,
22]. Those vegetation processes are mainly attributed to changes in soil hydrology and the active layer [
20,
23]. It was found that permafrost degradation wets the soils in lowlands and dries the surface soils in uplands or on slopes [
24] because of the different soil drainage in the active layer. In ice-rich lowlands at high latitudes, melting of ground ice and deepening of the active layer are associated with water-lodging conditions of soils in the active layer, because of the poor soil drainage and the relatively thin active layer [
23]. However, on uplands, a deepening active layer, as a result of the melting ground ice, increases downward infiltration of water in soil [
25] and decreases soil water content in the upper part [
18]. From the interactions between thawing permafrost and soil water, the relationship between vegetation growth and ALT weakens with a thickening active layer. In addition to soil water content, soil nutrient content is also associated with ALT, because nutrient cycles, including accumulation, leaching, and utilization, are all associated with the dynamics of plants, microbes, and soil hydrology [
26].
There have been several reports on the relationships between the ALT and vegetation in the Pan-Arctic regions. In comparison with that in arctic tundra, on average, the ALT is greater on the QTP due to its lower latitudes and stronger solar radiation [
14]. Previous studies on the QTP have documented that increase in ALT reduces vegetation cover and above-ground biomass [
27], with an ALT, or depth of the permafrost table, ranging from about 2 to 5 m; the greatest vegetation cover and biomass occurred in the areas with an ALT of about 2 m, and; vegetation cover, plant species diversity, and biomass decreased with the deepening active layer (from about 2 to 5 m) [
21], coupled with vegetation changes from alpine meadows dominated by cold-wet adapted species to alpine steppes dominated by warm-dry species, and even to alpine deserts [
5,
27]. However, the ALT for triggering vegetation succession and for different succession trajectories remains poorly understood, and little is known about the main influencing factors for vegetation in permafrost regions on the QTP [
28].
This study focuses on the ALT–vegetation relationship at high elevations (above 4289 m a. s. l.) with an ALT ranges of 0.6 to 3.5 m. Our hypotheses are: (1) Biomass, plant species diversity, and vegetation cover decrease with deepening active layer, and decrease progressively when the active layer is deeper than about 2.0 m; (2) Plant species composition is similar among sites with an ALT less than about 2.0 m; (3) Soil water content at vegetation root zone (30–40 cm) in the active layer, as well as seasonally frozen ground, is the main controlling factor for vegetation indices and plant species composition. The results will deepen our understanding of the relationship between plant community and the underlying permafrost under a warming climate.
4. Discussion
Previous studies have focused on the relationship between permafrost and vegetation in permafrost areas with greater ALT (>1 m); and in areas of seasonally frozen ground, the final stage of permafrost degradation has not yet been closely examined. In this study, areas with ALT ranging from 0.6 to 3.5 m were investigated to represent areas at different stages of permafrost degradation. Furthermore, vegetation indices and soil properties in areas of seasonally frozen ground were also analyzed, to explore the vegetation succession trajectories and the main influencing factors during the process of permafrost degradation. The distribution of permafrost and ALT in the HAYR change with elevation, slope aspects, substrates, soil water content, and vegetation [
48]. Thinner active layers are mainly distributed at higher elevations, with wetter, organically-richer, finer-grained soils, and with dense vegetation; while the seasonally frozen ground beneath alpine steppes is mainly distributed at lower elevations or on south-facing slopes, and soils are characterized by coarse sands and gravels, with good drainage conditions (
Table 1). In addition, in areas of seasonally frozen ground, at the sites with an organic layer or dense vegetation, mean annual ground temperature is lower compared with other sites, indicating the importance of the vegetation and organic layer in modifying ground temperatures [
49,
50].
4.1. Changes in Vegetation Characteristics with the ALT
At the permafrost sites, vegetation indices significantly changed with the increase of ALT, suggesting that permafrost degradation could lead to vegetation degradation. With the increase of ALT, plant cover, below-ground biomass, species richness and relative sedges cover decreased, while relative forb cover increased. Our results consist with other studies on the QTP showing that vegetation cover and below-ground biomass decreased with the increased of ALT [
22,
27], and the dominant species changed from the Cyperaceae to mesoxerophytes and xerophytes [
21]. Furthermore, our data also showed that vegetation indices changed dramatically when the ALT was more than 2.0 m, so as the vegetation composition, indicating that ALT was less than 2.0 m could maintain the alpine vegetation growth.
Indicator species analysis showed that
Carex spp. was the indicator species for permafrost sites, while
Potentilla bifurca Linn. was strongly correlated with sites at seasonally frozen ground. This is because in the zone of seasonally frozen ground,
Carex L. was absent, but
Potentilla bifurca Linn was common. This suggests that the decline of sedges over degrading permafrost may be mainly associated with the reduction of
Carex L. Generally, at our sites, sedges prefer wetter and colder habitats with a shallower active layer, while forbs dominated in warmer and drier habitats with a thicker active layer. This pattern can be explained in that a shallower active layer is generally associated with higher soil water content or even with saturation in soil profile with low oxygen availability. Sedges dominated in these low-oxygen or anaerobic conditions with a great quality of aerenchyma, which could transport oxygen downward to the root system, hence improving nutrient accessibility in soil [
51].
The NMDS analysis suggested that the vegetation composition was similar with an ALT is of less than 2.0 m and other vegetation indices like plant cover, relative cover of sedge and forb, and evenness would change dramatically with the ALT at 2.0–3.5 m. It has been documented that the vegetation cover and biomass were higher with the ALT at 2.0 m [
21], while a depth of permafrost table of less than 3.0 m would result in a high vegetation cover (> 85%) [
27]. In addition, a recent study showed a positive correlation between the below-ground biomass and the ALT in the upper Heihe River basin in the Qilian Mountains on the northeastern QTP [
14], in contrast to the results of this study. This can probably be attributed to the regional differences in climate and vegetation cover between the two study areas. The multi-year average of annual precipitation is 400 mm in the Heihe River basin, while it is 323 mm in our study area in the HAYR. On the other hand, the vegetation cover ranged from 64–94% in the upper Heihe River basin, while from 47–100% in the HAYR. In arctic tundra, a deeper active layer or thaw depth is generally associated with more aquatic species [
24,
52,
53,
54]. This is attributed to a much shallower, and generally wetter, active layer and poor drainage, resulting from thawing ice-rich permafrost in the arctic [
17,
55].
The above-ground biomass and relative forb cover in our study did not show a significant relationship with the ALT. This can be explained that climate warming could also increase forb abundance [
56]. Our sites, at lower elevations, could also be affected by grazing of large herbivores. Experimental studies indicate that grazing exclusion could increase the above-ground biomass, plant cover, and plant functional groups [
57].
4.2. Influencing Factors of Vegetation in Response to Permafrost Degradation
The relationship between ALT and vegetation has been attributed to the influence of soil hydrology and nutrient content on vegetation in permafrost regions [
14,
16,
53,
58]. Soil water contents at shallow depths (0–40 cm) are significantly higher at permafrost sites, while silt contents at depths of 20–30 and 30–40 cm, and soil nutrient contents are significantly lower at sites in the zone of seasonally frozen ground (
Figure 2). At permafrost sites, contents of soil water and major nutrients (TC, TN, and TP) significantly (
p < 0.05) declined with increasing ALT (
Figure 5), and they were much lower at sites with ALT greater than 2.0 m. This indicates an ALT of 2.0 m as the critical depth for maintaining the higher water content and nutrient availability for the upper part of soil layers (0–40 cm). In our case, sites with ALT less than 2.0 m were all located in flat areas with a thick organic layer (> 40 cm), and in alpine meadows with a vegetation cover greater than 90%. These observations about surface organic layer and vegetation explain the 2.0 m as the critical value of ALT in maintaining local soil hydrology for the underlying permafrost. Our results also showed that vegetation indices and species composition were strongly influenced by the physical properties (water content, pH, and silt content) and nutrient contents (TC, TN, and TP) of soils, as well as elevation (
Figure 6).
The results of step-wise multiple linear regressions (factors were water content of soil at different shallow depths) showed that plant cover, below-ground biomass, and relative cover of forbs and sedges are significantly influenced by soil water content at depths of 30–40 cm (
Table 6), revealing the importance of soil water content in the root zone of alpine vegetation on the QTP [
55,
59]. This suggests that even if ALT is greater than 2.0 m, the presence of permafrost may still benefit vegetation growth via the positive effects of higher soil water contents at 30–40 cm in soil depth. On the QTP, 86% of the sedge roots are distributed in the top 30 cm of soils [
60]. With deepening active layer, soil water infiltrates downward, resulting in drier soil at shallow depths, and possibly even mortality of wetland plants [
61]. Consequently, this may further result in a lower vegetation cover, species richness, and below-ground biomass; and furthermore, more shallow-rooted plants, for example, sedges would shift to deep-rooted plants, such as forbs [
55,
62], because of the better water uptake capacity of forbs [
63].
Soil pH and contents of silt, TC, TN, and TP significantly (
p < 0.05) increased with increasing soil water content (
Table 5), suggesting the association of all those soil properties with soil water content. Taking into account the correlations between vegetation and soil properties, it is evident that soil water content is the most important influencing factor for alpine meadow and steppe vegetation [
60,
64]. This is in agreement with the results from other studies on the QTP [
38,
57,
65].
In addition, vegetation is also strongly affected by elevation and microtopography (e.g., slope aspect) as well as other environmental factors [
66,
67]. There are associations of elevation with air temperature and precipitation, and slope aspect could influence soil drainage [
68,
69]. For example, in our study areas, the KQ2 and KQ4 sites were about a few hundred meters apart in the same basin. KQ4 is on a sunny slope (about 5°), while KQ2 is on the bottom of an intermontane basin. The vegetation at the KQ4 site is alpine desert with some drought-tolerant species dominated by
Artemisia sieversiana Ehrhart ex Willd. and
Saussurea hieracioides Hook. F. However, that at the KQ2 site is alpine meadow, dominated by
Kobresia sp. and
Polygonum sibiricum Maxim.
The distribution of vegetation and its influencing factors were identified in this study. We focused on the relationships between characteristics of vegetation and ALT at high elevations, above 4200 m a. s. l. However, due to the limited accessibility and the harsh field-work conditions for long-term monitoring, the total site numbers were limited to only 22 sites, and only 9 were in the arer of seasonally frozen ground. An implementation plan for long-term vegetation monitoring with more diverse sites, and the normality of the data for statistics in areas of permafrost and seasonally frozen ground, as well as talik zones, is required for better understanding of their relationships.
5. Conclusions
Our results showed that plant cover, below-ground biomass, plant species richness, and relative cover of sedges decreased with deepening active layer, while Pielou evenness and relative forb cover showed a contrary trend. All those abovementioned vegetation indices exhibited a significant decrease or increase at the ALT of 2.0 to 3.5 m. Furthermore, plant species composition was more similar at the ALT of less than 2.0 m, and with a thick organic layer and dense vegetation. In the areas of seasonally frozen ground, the dominant vegetation change from sedges to forbs and the Carex L. disappears totally. However, plant species were more diverse in the zone of seasonally frozen ground. The statistical analysis suggests that soil properties, including soil water content, pH, contents of silt (and TC, TN, and TP) in the active layer, and elevation, were responsible for changes in vegetation over degrading permafrost. Especially, soil water content at depths of 30–40 cm was the most important factor for vegetation succession. We concluded that an ALT greater than 2.0 m over permafrost could still maintain higher contents of soil water and nutrients for the vegetation root zone to sustain vegetation growth.
This study could help better understand the impact of increasing ALT on vegetation growth and composition, and allow a better prediction of vegetation succession above degrading permafrost. The impact of ALT on vegetation was studied, however, without accounting for changes in precipitation due to the limited meteorological stations or rain gauges in our study area. Because the crucial role of soil moisture content in influencing vegetation features is crucial, it is clear that the vegetation degradation is not only resulted from the thickening active layer; changes in precipitation also greatly impact alpine vegetation. Under a changing climate, especially those that are warmer and wetter climate, long-term monitoring and regional studies on the impacts of permafrost degradation, are urgently needed along with research on the dynamics of the supra-permafrost water table with alpine vegetation on the QTP, are urgently needed for scientific management, and prudent protection, of alpine ecosystems.