Plant diversity is closely related to the density of zokor mounds in three alpine rangelands on the Tibetan Plateau

Study site

The study sites were selected from three representative rangeland types with typical features of plant community inhabited by plateau zokors in the north-eastern of the Tibetan Plateau: alpine meadow, alpine steppe and alpine shrub meadow. These three sites are about 300 km apart from each other (Fig. 1).

The alpine meadow was in Tianzhu Tibetan County at 37°10′33.01″N and 102°49′54.32″E and with an elevation of 2,823 m. The mean annual temperature is −0.6 °C in the past several years, and the mean annual rainfall is 416 mm, which mainly distributes in July–September. The soil is classified as alpine meadow soil. The average diameter of single plateau zokor mound was around 60 cm and the average height was 30 cm, which is largest and highest in the three alpine rangelands. The dominant species in this study site are Kobresia capillifolia, Kobresia humilis, Carex lanceolata, Elymus nutans, Poa pratensis and Koeleria cristata.

The alpine steppe was in Sunan County, Zhangye at 39°30′57.23″N and 98°09′58.57″E and an elevation of 3,458 m above sea level. The mean annual temperature is −1.2 °C in the past several years; the mean annual rainfall is 252 mm. The soil is classified as alpine steppe soil. The average diameter of single plateau zokor mound was around 20 cm and the average height was 10 cm, which is smallest mound in the three alpine rangelands. The dominant species in this study site are Poa annua, E. nutans, Stipa capillata and Achnatherum splendens.

The alpine shrub meadow was in Sunan County, Zhangye at 38°46′21.85″N and 99°49′13.15″E and an elevation of 3,189 m above sea level. It has a mean annual temperature of 2 °C and a mean annual rainfall of 350 mm in the past several years. The soil is classified as mountain chestnut soil. The average diameter of single plateau zokor mound was around 40 cm and the average height was 20 cm, which is medium sized mound in the three alpine rangelands. The dominant species in this study site are Potentilla fruticosa, Polygonum viviparum and Kobresia capillifolia. The basic information of these study sites is shown in Table 1.

Experimental design

Survey of plateau zokor mound density and gradient division

We consulted technicians at local rangeland stations and herdsmen, and selected areas where plateau zokors are the only single subterranean rodent species with a residence period of more than 10 years. Three replicate gradient plots were selected for each rangeland type, and five adjacent areas with different mound densities were selected from each plot. The area of each density gradient zone was 2,500 m² (Fig. 2A), and the number of new and old plateau zokor mounds in the plots was counted by the artificial counting method. New mounds were those that had recently been formed, within a year, excavation by plateau zokors and without vegetation cover (bare land). Old mounds were more than 2 years old and were covered with vegetation. Mound density was calculated from the total number of old and new mounds. The rangeland without zokor mounds was used as a control (CK), and the plots were classified as plots A, B, C and D with the density of zokor mounds increased. Soil and plant sampling were conducted in non-mound areas, as show in Figs. 2B and 2C. The number of zokor mounds in different plots was show in Table 2. The field work was permitted by College of grassland Science of Gansu Agricultural University.

Table 2:

The number of zokor mounds in different mounds density plots on the three alpine rangelands.

Plots	Alpine meadow		Alpine steppe		Alpine shrub meadow
	New mounds	Old mounds	New mounds	Old mounds	New mounds	Old mounds
CK	0.00	0.00	0.00	0.00	0.00	0.00
A	4.67 ± 1.25	15.00 ± 3.74	82.67 ± 10.50	160.67 ± 8.22	16.67 ± 5.31	23.33 ± 4.03
B	14.00 ± 3.74	28.00 ± 6.53	181.33 ± 14.38	173.00 ± 6.48	26.00 ± 4.90	70.67 ± 8.22
C	21.00 ± 2.94	57.67 ± 8.65	331.67 ± 22.69	217.00 ± 12.03	33.00 ± 2.94	124.67 ± 9.53
D	45.00 ± 6.16	103.67 ± 12.92	439.33 ± 28.57	222.00 ± 9.27	83.00 ± 11.43	323.67 ± 18.45

DOI: 10.7717/peerj.6921/table-2

Note:

The values represent mean values (±SE).

Data analysis

In the three alpine rangelands, we first analyzed changes in plant diversity and soil moisture and temperature in relation to the different mound densities. Multiple comparisons were made for species richness, abundance, Simpson, Shannon, soil temperature and moisture between different mound density zones in different rangeland types using the least significant difference method. The cumulative species richness was compared between different mound densities using species accumulation curves, and the species abundance distribution within the community was assessed by the species abundance rank. Plant species were classified into five functional groups (grasses, sedges, perennial forbs, annual forbs and shrubs, Klein, Harte & Zhao, 2007), and the functional group data were expressed as the sum of the importance values of the different species within the functional group. Changes in the functional groups with increasing zokor mound density were analyzed in different alpine rangelands. Finally, a structural equation model was constructed to quantify the direct and indirect effects of zokor mounds and soil moisture and temperature on plant diversity.

Effect of plateau zokor mounds on plant diversity in the three rangelands

In the alpine meadow, the species richness and the Shannon and Simpson indices of the plant communities increased significantly with the increasing density of the plateau zokor mounds. The species abundance was not affected by mound density (Fig. 3). In the alpine steppe, the species richness and Shannon and Simpson indices of the plant communities decreased significantly with increasing mound density (Fig. 3). In the alpine shrub meadow, the species richness and Shannon and Simpson indices of the plant communities in non-mound areas first increased and then decreased with increasing mound density. There was no significant relationship between species richness and mound density (Fig. 3).

Effect of plateau zokor mounds on soil temperature and moisture in three rangelands

In the alpine meadow, soil temperature at the 0–10 cm layer did not change significantly with increasing plateau zokor mound density, whereas there were significant decreases at the soil layer of 10–20 and 20–30 cm. Meanwhile, soil moisture increased significantly at the soil layer of 0–10, 10–20 and 20–30 cm (Fig. 4).

In the alpine steppe, the soil temperature at the depths of 0–10, 10–20 and 20–30 cm decreased significantly with increasing density of plateau zokor mounds. In contrast, soil moisture at the depths of 0–10 and 20–30 cm increased significantly, but no significant change occurred at the depth of 10–20 cm (Fig. 5).

In the alpine shrub meadow, the soil temperature at the depths of 0–10, 10–20 and 20–30 cm decreased significantly with the increasing density of plateau zokor mounds. In contrast, the soil moisture at the depths of 10–20 and 20–30 cm increased significantly, but there was no significant change in soil moisture at the depth of 0–10 cm (Fig. 6).

Changes in cumulative species richness with different mound densities and abundance distribution in the three rangelands

Figure 7A shows the accumulation of species richness with different mound densities in the three rangeland types. In the alpine meadow, the cumulative species richness and the accumulation rate were increased with increasing mound density. In the alpine steppe, the above two parameters first decreased and then increased with increasing mound density. In the alpine shrub meadow, these two parameters initially increased and then decreased with increasing mound density.

In the alpine meadow, all the species abundance distribution in the alpine meadow could be fitted by the logseries model with R² > 0.93. Furthermore, species abundance distribution was relatively even. In the alpine steppe, the fitted curves were relatively steep. All the species abundance distribution in the alpine steppe could also be fitted by the geometric model with R² > 0.79. In the alpine shrub meadow, the fitted curves were also relatively even. All the species abundance distribution in the alpine shrub meadow could also be fitted by the logseries model with R² > 0.87 (Fig. 7B). Above all, the species number that predominantly structure the plant community was fewer in the alpine steppe than alpine shrub meadow and alpine meadow.

Changes in functional group composition with different mound densities in the three rangelands

In the alpine meadow, the proportion of grasses decreased with increasing mound density, while the proportions of sedges, perennial forbs and annual forbs increased; annual forbs showed the highest rate of increase (Fig. 8A). In the alpine steppe, there was no clear trend of change in the proportion of different functional groups with increasing mound density. However, the proportion of perennial forbs increased (Fig. 8B). In the alpine shrub meadow, the proportion of shrubs first decreased and then increased with increasing mound density, while the proportion of perennial forbs first increased and then decreased (Fig. 8C).

The effects of zokor mounds to soil properties and plant diversity in the three rangelands

In the alpine meadow, the direct effect of zokor mounds on soil properties was 0.84, and the direct effect on plant diversity was 0.86 (Fig. 9A). In the alpine steppe, the direct effect of zokor mounds on soil properties was 0.87, and the direct effect on plant diversity was 0.17 (Fig. 9B). In the alpine shrub meadow, the direct effect of zokor mounds on soil properties was 0.74, and the direct effect on plant diversity was 0.24 (Fig. 9C). Soil moisture and temperature was significantly affected by zokor mounds. Among the three rangeland types, zokor mounds had the greatest effect on plant diversity in the alpine meadow.

The indirect effects of zokor mounds on plant diversity are directly realized through creating greater spatial heterogeneity

Subterranean rodents, one of the most important components of rangeland ecosystems, are regarded as ecosystem engineers that greatly influence ecological processes such as soil nutrient cycling, spatial heterogeneity and plant diversity (Hu et al., 2017; Reichman & Seabloom, 2002; Smith & Foggin, 1999; Zhang, Zhang & Liu, 2003). Subterranean rodents show different degrees of importance and irreplaceability compared with aboveground herbivores. Mielke (1977) believed that subterranean rodents are the most direct drivers of change in soil chemical properties in North American rangelands and that their underground excavation activity is important for soil nutrient cycling. Grinnell (1932) concluded that plant diversity would rapidly decline in the region if populations of subterranean rodents went extinct. Subterranean rodents dig burrows and push soil toward the ground surface to form mounds, this is the most direct and obvious effect of such animals on soil and plant communities (Smith & Foggin, 1999; Thorn, 1978). Mound creation considerably changes the microtopographic features of the land surface and leads to the redistribution of soil temperature and moisture. Because mounds are significantly higher than the surrounding non-mound area, rainwater accumulates in the low-lying area. Additionally, the mounds change the light conditions in the surrounding area to some extent, thereby changing soil temperature. Plateau zokors, a unique rodent species that lives underground on the Tibetan Plateau, are mainly distributed in alpine meadow, alpine shrub meadow and alpine steppe areas (Cai et al., 2018; Zhang, Zhang & Liu, 2003). There is no scientific basis for that plateau zokors compete with livestock for food resources and cause soil erosion and rangeland degradation. The local government and herdsmen organize to eradicate zokors every year and hope to completely eliminate this species (Zhang, Zhang & Liu, 2003). But the animals are capable of changing the physical conditions of their living environment and thus created high heterogeneity environment, and then strongly affect the distribution of other organisms. Environments with high heterogeneity created an ecological condition where presenting a wider range of niches, and more species as a consequence. The results of this study showed that the soil temperature in non-mound areas decreased with increasing mound density, while the soil moisture increased in the three rangeland types on the Tibetan Plateau, indicating that the formation of mounds by plateau zokors led to the redistribution of soil moisture and temperature. Hu et al. (2017) also concluded that plateau zokors had greatly direct impact on the soil physiochemical properties through their foraging and burrowing activities. Wang et al. (2008) found that zokor disturbance resulted in a significant change in soil particle size, increased soil water content from 20% to 25%. In this study, structural equation modeling also revealed highly significant effects of mounds on soil moisture and temperature and then on plant diversity in the three rangeland types (Fig. 9). This suggests that the indirect effects of zokor mounds on plant diversity are directly realized through creating greater spatial heterogeneity (such as soil temperature and moisture).

The direct effects of zokor mounds on plant diversity maybe realized through cyclic succession on bare mound patch

Plateau zokor mound is a common disturbance in the alpine rangeland ecosystem (Hu et al., 2017; Wang et al., 2008; Yang et al., 2017; Zhang et al., 2012). Zokor mounds make the plant communities in alpine rangelands spatially heterogeneous and dynamic mosaic communities. Our study showed that the plant diversity increased significantly in the alpine meadow and decreased significantly in the alpine steppe with increasing mound density, but it initially increased and then decreased in the alpine shrub meadow. The results of the structural equation model showed that zokor mounds directly affected plant diversity significantly in different types of alpine rangeland on the Tibetan Plateau. The plant diversity showed different trends of change with increasing mound density among the different rangeland types, and the trends of change in a plant community as a result of a zokor mounds disturbance may be explained mainly by a direct mechanism. That is, within short periods, new zokor mound that randomly generated undergo secondary succession in local areas. These new mounds eventually form stable communities that are mosaics of different types of communities. There is thus a cyclic series from bare mounds to climax community then to bare mounds. Yang et al. (2017) also concluded that there was much variation in species composition at earlier stages of succession on the bare mounds, but communities on older mounds became more similar to each other and to their surrounding vegetation over the course of secondary succession. The alpine steppe is a fragile rangeland ecosystem with a thin soil layer and low soil nutrients, and low soil moisture and low plant density. Owing to the harsh environmental conditions, the species abundance distribution curve was steepest for the plant community, indicating that plant communities were dominated by the dominant species in this ecosystem which resulted in low species richness. Because the non-mound areas are considered dynamic mosaic plant communities resulting from succession toward a stable state from bare mound patches formed in different periods, the current climax community have undergone multiple succession processes from bare mound patches. During each cyclic succession, the dominant species become more abundant, thus reducing the diversity of the alpine steppe and even causing irreversible degeneration. Therefore, the control and prevention of zokor should be strengthened in the alpine steppe. In contrast, the alpine meadow and alpine shrub meadow have better environmental conditions, including a thicker soil layer and higher soil nutrient contents as well as a high density of vegetation that can be rapidly restored. Thus, these two ecosystems can resist a certain degree of disturbance from zokor mounds. In these two ecosystems, the abundance distribution curve of the community was relatively flat. Because the available resources for plants are abundant, the interspecific competition in the plant communities is relatively low. Due to the dynamic mosaic of plant communities, each plant species has an equal opportunity to colonize bare mound patches during the succession process, so the climax community accommodate richer plant communities in the alpine meadow. Because mixed small communities are more diverse than single large communities (Begon, Townsend & Harper, 2006), so the alpine meadow has higher plant diversity. Moreover, the cumulative species richness also increased with increasing mound density in the alpine meadow (Fig. 7), further indicating that zokor mounds increased the heterogeneity of plant communities. This study also resulted that “opportunistic” annual plants increased the fastest with increasing mound density in the alpine meadow (Fig. 8). Plant diversity showed unimodal changes with increasing mound density in the alpine shrub meadow, and this may be because the alpine shrub meadow contains higher soil moisture per se, while the formation of zokor mounds further increases soil moisture. This could limit some mesophytic and xenobiotic plants, so plant diversity would initially increase and then decrease with increasing mound density. The possible mechanisms by which zokor mounds directly affect plant diversity may be explained by the fact that the time and potential of cyclic succession on the bare mound patches are different.

Zokor mounds disturbance on alpine rangeland can deepen our understanding toward co-evolved process

Disturbances constituting a series of events play a significant role in the structure and function of ecosystems (Battisti, Poeta & Fanelli, 2016c; Dornelas, 2010; Mackey & Currie, 2001; Sousa, 1984). A first substantial distinction of disturbance typologies can be classified into biotic disturbances and abiotic disturbances. Disturbances caused by animals are usual in various natural environments and are associated to the different functions carried out by living organisms over their daily, seasonal, annual and life cycles (Brawn, Robinson & Thompson, 2001; Gibson, 1989; Sousa, 1984). Such disturbances can be classified into five popular types at least: trampling, foraging, tunnel digging, feces and urine deposition (Battisti, Poeta & Fanelli, 2016a). Due to the year-round subterranean life of some rodents, so there are no trampling effects. The disturbances induced from animal can be recognized as significant agents of natural selection. They play a very important role in changing the structure, composition, diversity, distribution and the long-term co-evolution dynamics of plant and animal (Dornelas, 2010). Herbivorous and subterranean rodents are widely distributed around the rangeland regions of the earth except two continents (Australia and Antarctica) (Andersen, 1987). The plateau zokors, which are the only small herbivorous subterranean mammal on the Tibetan plateau, may have great effects on the alpine ecosystem in different kinds of ways because of their specific behavioral pattern, lifestyle and population dynamic (Wang et al., 2008; Yang et al., 2017). In China, plateau zokors have been conventionally regarded as pests and elimination projects have been implemented by local governments because they competed with cattle, and caused soil erosion to a certain degree (Smith & Foggin, 1999; Zhang, Zhang & Liu, 2003). The change of plant community composition and the maintenance of species diversity in alpine rangeland as a result of zokor mounds disturbance can be explained mainly from three aspects (Fig. 10). Tunnel digging is the main activity performed by alpine zokor to affect ecosystems, resulting in the formation of micro-topography and gap. The foraging of zokor belongs to below-ground foraging; it is difficult to quantitatively evaluate the impact of zokors foraging on the alpine rangeland. So, we focused attention on the tunnel digging and mound making activities. Future work should quantitatively study the zokor foraging by using stable isotope techniques. We can then evaluate the effects of zokor foraging to rangeland ecosystem. We emphasize the key role of plateau zokors play on the rangeland ecosystem of Tibetan plateau. We reckon plateau zokor to be a keystone species because: (1) it makes mounds that are the primary habitat to a great range of niches for plants living; (2) it creates micro-topography that results in the increasing of plant micro-patches; (3) it will be conducive to plant community and ecosystem-level dynamics; (4) underground excavation activity is important for soil nutrient cycling. But disturbance by zokor mounds has different effects on plant diversity in different ecosystems and the anti-interference ability of the Tibetan Plateau. Zokor mounds lower the species diversity of plant communities in the fragile alpine steppe while laying a foundation for the co-existence of various species in plant communities and the maintenance of plant diversity under favorable alpine ecosystem (Fig. 10). In order to ensure the lasting sustainable use of alpine rangeland on Tibetan Plateau accompanied by the equilibrium of ecosystem and conservation of native biological diversity, plateau zokors should be managed jointly with other integrated management approach on the alpine rangeland ecosystem.