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Response of alpine meadow communities to burrow density changes of plateau pika (Ochotona curzoniae) in the Qinghai-Tibet Plateau
Acta Ecologica Sinica 32 (2012) 44–49
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Response of alpine meadow communities to burrow density changes of plateau pika (Ochotona curzoniae) in the Qinghai-Tibet Plateau Zheng Gang Guo ⇑, Xiao Feng Li, Xing Yuan Liu, Xue Rong Zhou State Key Laboratory of Grassland Farming Systems, College of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou, China
a r t i c l e
i n f o
Keywords: Plateau pika Available burrow density Alpine meadow Qinghai-Tibetan Plateau
a b s t r a c t Plateau pika (Ochotona curzoniae) is a key component of alpine meadow ecosystem in the QinghaiTibetan Plateau, and the increase of its number leads plant components of alpine meadow ecosystem to adaptively response. A field survey was carried out to determine the response of alpine meadow community to population densities of plateau pika by using available burrow density to replace the population density of plateau pika. This study showed that the height of alpine meadow communities gradually increased, and the cover of alpine meadow communities firstly decreased, and then increased as the available burrow density increased. With the increase of available burrow density, the richness index of alpine meadow communities firstly decreased and then increased, and the evenness index of alpine meadow communities firstly increased and then decreased, however, the diversity index of alpine meadow communities firstly increased, and then decreased, finally increased. In the increasing process of available burrow density, the total plant biomass and the unpalatable plant biomass firstly decreased and then increased, and the palatable plant biomass firstly increased and then decreased, indicating that the palatable plant biomass was the highest and the unpalatable plant biomass was the lowest at 14 available burrow per 625 m2. In the economic groups of plant biomass, the weed biomass was the highest and the legume biomass was the lowest at any available burrow densities, and the grass biomass and the sedge biomass were related to available burrow densities, indicating that the sedge biomass were bigger than the grass biomass at 3 available burrow per 625 m2, inverse at 54 available burrow per 625 m2, similar between 3 and 34 available burrow per 625 m2. Accompanying by the increase of available burrow densities, the legume biomass and the sedge biomass significantly decreased (P < 0.05) and the legume became disappearance at 54 available burrow per 625 m2; the grass biomass firstly increased and then decreased, peaking at 14 available burrow per 625 m2. The weed biomass firstly decreased and then increased, and was the lowest at 14 available burrow per 625 m2. This study suggested that the responses of alpine meadow communities to population density of plateau pika at 14 available burrows per 625 m2 were more sensitive than that at other available burrow per 625 m2 from plant species diversity, biomass, height, cover and economic group. Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction The continual increase in population density of the plateau pika (Ochotona curzoniae) develops a rat trouble, which threatens the health of alpine meadow ecosystem and the development of animal husbandry economy in the Qinghai-Tibetan Plateau, but the plateau pika is a survival animal component of alpine meadow ecosystem in the process of ecosystem evolution. Previous studies have proven that the plateau pika plays the negative and positive roles in meadow alpine ecosystem, which depends on its population density [1]. The right density of plateau pika not only provides foods for endemically carnivorous mammal and raptor which lives
⇑ Corresponding author. Tel.: +86 931 8913247. E-mail address: [email protected] (Z.G. Guo).
in the Qinghai-Tibetan Plateau [2], but also acts as disperse carrier of plant seeds, which encourages some plants to expanse their distribution [1,3]. The burrow produced by plateau pika not only increases the conservation water ability of alpine meadow by enabling more rainfall to permeate into deep soil, which increases water supplies for plant growth [4], but also provides habitats, reproductive place and shelter for insects, lizard and snow finch [1]. The plateau pika has presently been considered as a keystone species in the alpine meadow ecosystem [2], and the great change of its population density generally causes the structural and functional variation of alpine meadow ecosystem. The lower density of plateau pika weakens its basically connecting link between the preceding and the following creature in the food web of alpine meadow ecosystem, however, its higher density often causes a rat trouble by competing food resources with livestock and destructing the soil structures with burrowing behavior. From self-control
1872-2032/$ - see front matter Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2011.12.002
Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49
view of ecosystem, the increase or decrease of plateau pika density arouses the changes of vegetation components in the alpine meadow ecosystem, inversely; the vegetation degradation or improvement often adjusts the plateau pika density. Therefore, the aim of plateau pika control is to keep its density into a rational density rather than never-ending decrease its density. Plant community is the core component of alpine meadow ecosystem, and its structure and components varies with the changes of plateau pika density because the activities of plateau pika increase the environmental heterogeneity [2,5] and distribution area of some spermatophyte [6], inhibits some specific plant growth due to selective intake of plateau pika [1]. The structural changes of plant community affect the habitats of plateau pika, and further affect the migration behavior of plateau pika. Previous studies have shown that the plateau pika considers the higher height and cover vegetation as a predation risk, and lives in the habitat with low vegetation height and cover, even in the habitat with bare patch [7]. Therefore, understanding the relationship between plant community and density changes of plateau pika will provide useful profile for quantifying the appropriate population density of plateau pika to control this small manual. The objective of this study is to determine the effect of density changes of plateau pika on alpine meadow communities in the Qinghai-Tibet Plateau by using available burrow density substituting for plateau pika density.
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recorded by closing burrow exit for three days in May, 2009, and the distance between plots was over 50 m. According to available burrow number in plot, the plots was divided into four categories, in which 3(3 ± 1), 14(14 ± 2), 34(34 ± 3), and 54(54 ± 4) available burrow density per 625 m2 were finally selected to investigate the response of alpine meadow communities to available burrow densities of plateau pika, and each category was three plot as replicates. 2.3. Field survey and sampling The field survey was conducted from late July to early August in 2009. In each plot, five subplots with the size of 1 m 1 m were designed with ‘‘W’’ pattern distribution to collect quantitative data on the vegetation and distance between subplots was over 10 m. The total number of subplots was 60. In each subplot, present species number, total biomass and every species biomass (g), vegetation height and every species height (cm), total cover and every species cover (%) were recorded. The total foliage cover was measured by using 100 points (1 mm wire). Vegetation height was measured by lowering a perforated foam disc (diameter 0.1 m, weight 7 g) onto the vegetation along a gauged stick. Aboveground materials of all plants rooted in each subplot were collected by single species, and carried back, and then dried at 80 °C for 24 h and weighed in the laboratory. Subplot data within each plot were pooled. 2.4. Data analysis
2. Methods and materials 2.1. Study area The study was carried out in the Dawu town of Maqin County, Qinghai Province (32°310 –35°31, 96°540 –101°510 ). The study area locates in the Yellow River source area of Qinghai-Tibetan Plateau with the average elevation from 3874 m to 3780 m. The annual mean precipitation is 528.5 mm, mainly taking place during the period June to September, and the annual evaporation is 2470 mm. The mean temperature is -3.9 °C without free frost period. The climate in this area is plateau continental climate, in which spring, summer, autumn and winter is not identified, and the climate is divided into short warm season (from June to September) and long cool season (from October to May). The accumulative temperature with P5 °C is 850 °C and the period of plant growth is only 156 d. The soil is alpine meadow soil and alpine bush meadow soil with 30–50 cm thick [4], and their parent materials are chiefly residual deposits with coarse texture, consisting mostly of sand. Original vegetation is alpine meadow, which is dominated by Kobresia humilis with the main associate plant species of Kobresia pygmaea, Kobresia capillifolia, Aconitum szechenyianum, Stekkera chamaejasme, Ligularia virgaurea, Oxytropis coerulea, Elymus nutans, Poa annua, Stipa aliena, Leontopodium leontonpodioides, Ajuga lupulina, Artemisia nanschanica and Potentilla sp. 2.2. Experimental design A field survey was carried out on the cool season rangeland to avoid the effect of grazing on alpine communities in the process of survey, in which the yak and Tibetan sheep was grazed from middle October to early April, and rangeland during warm season is close grazing. It is difficult to determine plateau pika density by recording its number due to its family life pattern, therefore, the available burrow density of plateau pika was used to substitute for its own density. The higher available burrow density meant the higher plateau pika density [8]. Forty survey plots with the size of 25 m 25 m (625 m2) was randomly selected on the similar meadow flat and the available burrow density in each plot was
Importance value of species was calculated with the equation, IV = (relative height + relative cover + relative biomass)/3, and it was used to determine the dominant species and associate species. Three indices were chosen for estimation of a diversity [9], (1) the richness index (S) is represented by number of species recorded in each subplot; (2) the diversity index was measured P by the Shannon–Wiener’s index of diversity, H ¼ ni¼1 Pi LnPi i; and (3) the evenness index was measured by the Pielou’s index of evenness, J sw ¼ H=LnS, where Pi ¼ N i =N; Ni is the importance value of individual species i; N is the total individuals of all species present; S is number of vascular species present. Based on principle of grassland utilization, the plant in subplot was divided into four economic groups, including grass group, sedge group, legume group, and weed group [10]. Differences in plant species diversity, cover, biomass, and soil parameters among alpine meadows of four available burrow densities were analyzed by using one-way ANOVA. 3. Results 3.1. Effect of available burrow densities on component and vertical structure of plant communities The number of plant species ranged from 43 to 32 in the subplot, and firstly increased and then decreased as the available burrow density increased (Table 1). Although the dominant species always was K. humilis, the associate species obviously changed with the increase of the available burrow density, indicating that A. szechenyianum at 3 available burrow density per 625 m2 was replaced by S. chamaejasma at 14 available burrow density per 625 m2, and replaced by L. virgaurea and O. coerulea at 34 and 54 available burrow density per 625 m2, respectively. The change of associate species in plant communities resulted in difference of family and genus. The number of plant species and genus in the subplots firstly decreased and then increased, and was the lowest at 34 available burrow density per 625 m2; however, the number of family in the subplots firstly increased and then decreased, peaking at 14 available burrow density per 625 m2.
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Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49
Table 1 Effect of available burrow densities of plateau pika on community structure of alpine meadow. Burrow densities (number/ 625 m2)
Dominant species
Associate species
Species number Familia
Genus
Species
3 14 34 54
Kobresia Kobresia Kobresia Kobresia
Aconitum szechenyianum, Kobresia capillifolia Stellera chamaejasma, Leontopodium alpinum Ligularia virgaurea, Artemisia nanschanica Oxytropis coerulea, Ajuga lupulina
16 20 16 16
38 33 29 30
43 37 32 35
humilis humilis humilis humilis
The available burrow density greatly affected the vertical structure of plant communities. The plant communities at 3 available burrow density per 625 m2 were double layers, in which A. szechenyianum occupied the upper layer and the plants from sedge family grew at low layer. At 14 available burrow density per 625 m2 conditions, the upper layer was occupied by grass and S. chamaejasma and the low layer was took up by plant from sedge genus and low weeds. The vertical structure of plant communities varied with the growing season of main associate plants when the available burrow density was over or equal to 34 burrow density per 625 m2, indicating that the plant communities were single layer when L. virgaurea and O. coerulea was vegetative growth stage and they were double layers when L. virgaurea and O. coerulea entered into reproductive growth stage. 3.2. Effect of available burrow densities on height and cover of plant communities The height of plant communities decreased as the available burrow density increased (Fig. 1A), indicating that the height of plant communities at 3 available burrow density per 625 m2 was significantly bigger than that at 34 and 54 available burrow density per 625 m2 (P < 0.05). The cover of plant communities firstly decreased and then increased with the increase of available burrow density
A
Vertical structure
2 2 1or 2 1or 2
(Fig. 1B), and it was the lowest and was over or equal to 80% at 14 available burrow density per 625 m2. 3.3. Effect of available burrow densities on species diversity of plant communities With the increase of available burrow density, the richness index of plant communities firstly decreased and then increased (Fig. 2A), indicating that the richness index at 34 available burrow density per 625 m2 was the lowest and significantly lower than that at other burrow densities per 625 m2 (P < 0.05). The evenness index of plant communities firstly increased and then decreased as the available burrow density increased (Fig. 2B), and it peaked at 14 available burrow density per 625 m2 and was significantly bigger than that at 3 and 54 available burrow density per 625 m2. The diversity index of plant communities was not different between 14 burrow number per 625 m2 and 54 available burrow number per 625 m2, and they were significantly bigger than those at 34 and 3 available burrow number per 625 m2 (Fig. 2C). 3.4. Effect of available burrow densities on biomass of plant communities The total plant biomass firstly decreased and then increased as the available burrow density increased (Fig. 3A), and was the lowest at 14 available burrow densities per 625 m2. The palatable plant biomass was not consistent with the unpalatable plant biomass (Fig. 3B). The palatable plant biomass increased from 3 available burrow density per 625 m2 to 14 available burrow density per 625 m2 and decreased when the available burrow density per 625 m2 was over 14, and the unpalatable plant biomass firstly decreased and then increased with the increase of available burrow density, and was the lowest at 14 available burrow density per 625 m2, and these implied that the increase of available burrow density changed the total biomass and palatable biomass, in which 14 available burrow density per 625 m2 was points of inflection point. 3.5. Effect of available burrow densities on economic groups of plant communities
B
Fig. 1. Effect of available burrow densities of plateau pika on height (A) and cover (B) of alpine meadow.
The biomass of weed group accounted for the largest percentage of the total plant biomass at four available burrow densities (Table 2), mainly consisting of Delphinium grandiflorum, Ajania purpurea, Pedicularis kansuensis, A. szechenyianum, L. virgaurea; however, the biomass of legume group mainly deriving Astragalus membranaceus and Gueldenstaedtia verna was the lowest. The percentage of grass and sedge group biomass in the total plant biomass varied with the increase of available burrow density. The biomass of sedge group was bigger than the biomass of grass group at 3 available burrow density per 625 m2, and was lower than the biomass of grass group at 14 available burrow density per 625 m2, and the biomass of grass and sedge group was similar when available burrow density was over or equal to 34 available burrow density per 625 m2. The biomass of legume group significantly decreased as the available burrow density increased
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Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49
A
30
a
A
b
a
180
20 15 10
ab
b
b
150
Total biomass (g/m2)
25
Richness index
ab
ab
120 90 60 30
5 0 3
0 3
14
34
54
14
34
54
Available burrow densities (number/625m2)
Available burrow densities (number/625m2)
Evenness index
1
160
Palatable
140
b
a
ab
b
0.8 0.6 0.4
Biomass (g/m2)
B
B
1.2
a
a
a
Unpalatable
120
b
100 80 60
a
b
c
40
c
20 0 3
0.2
14
34
54
Available burrow densities (number/625m2) 0 3
14
34
54
Available burrow densities (number/625m2)
C
3.5 3
Diversity index
Fig. 3. Effect of available burrow densities of plateau pika on the total biomass (A), and palatable and unpalatable biomass (B) of alpine meadow community (The same bar with the different a, b and c means significant difference at 0.05 level).
b
a
3
14
b
a
2.5 2 1.5 1 0.5 0
34
54
Available burrow densities (number/625m2) Fig. 2. Effect of available burrow densities of plateau pika on the richness index (A), evenness index (B), and diversity index (C) of alpine meadow community.
(P < 0.05) and disappeared at 54 available burrow density per 625 m2. The biomass of weed group firstly decreased and then increased with the increase of available burrow density, and was the lowest at 14 available burrow density per 625 m2. This study showed that the most sensitive response of weed, sedge, grass group to available burrow density was 14 available burrow densities per 625 m2. 4. Discussions 4.1. Relationship between the available burrow density and the structure and productivity of alpine meadow The activities of plateau pika redistribute the light energy and water resources to various extent in the land surface and soil when
the plateau pika enters into slightly degraded alpine meadow, which affects the plant growth consisting of plant communities by directly or indirectly ways [7], sometimes, developing a shortterm stability habitat. This habitat often varies with the increase of plateau pika density. This study suggests that the available burrow density affect the primary productivity of alpine meadow by changing the vertical structure, plant species number, height, cover and biomass. The disturbance of plateau pika activities on alpine meadow is very weak at 3 available burrow density per 625 m2; consequently, the alpine meadow maintains its own features and productivity. At 14 available burrow density per 625 m2, the vegetation cover decreases because the more plant was grazed and buried by plateau feeding and burrowing behavior. With the further increase of available burrow density, the bare patch increases [8], and this provides invasion changes for opportunistic species, especially broad-leaves plant, resulting in increasing the vegetation cover. The plateau pika affects the vertical structure of alpine meadow community by causing the replacement of associate species, and the growth stages of these associate species regulates the vertical structure. At 34 available burrow density per 625 m2, the vertical structure of alpine meadow community changed from single layer into double layers when L. virgaurea grows from vegetative stage with low height to reproductive stage with the high height, and this implies that the influence of plateau pika on the vertical structure of alpine meadow community is related to sample time because the height of broad-leaved plant was different between vegetative stage and reproductive stage [11]. As the available burrow density increases, the total biomass and unpalatable biomass firstly decreases and then increases, and the palatable biomass shows a inversely trend, at the same time, the biomass of weed group accounts for the biggest percentage of the total biomass, and these imply that the total biomass of alpine meadow is determined by weeds not palatable plant and the
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Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49 Table 2 Effect of available burrow densities of plateau pika on economic groups of alpine meadow (g/m2). Burrow densities (number/ 625 m2)
Grass
Sedge
Legume
Weed
3 14 34 54
11.75 ± 1.23c 30.26 ± 2.34a 12.39 ± 1.98c 16.75 ± 2.01bc
46.09 ± 3.21a 28.12 ± 2.41b 13.67 ± 1.89c 11.94 ± 2.12c
1.88 ± 0.23a 1.52 ± 0.12b 0.99 ± 0.08c 0
104.99 ± 10.36b 81.02 ± 4.52c 121.51 ± 9.56a 124.43 ± 11.23a
Note: The data means the average value ± SE, and the data with the same letter in a column was not significantly different at 0.05 level.
activities of rational plateau pika improve the quality of alpine meadow [10] by increasing the palatable biomass. Alpine meadow maintains its own competition pattern of plant populations because the plateau pika has limited influence over alpine meadow when its density is low [12], in which A. szechenyianum is mainly associate species with high height and rich leaves and stems. The increase of available burrow density encourages S. chamaejasma and L. alpinum with low height to replace the A. szechenyianum and to become the mainly associate species, which provides the good light for palatable sedge plant growing at the low layer, resulting in increasing the palatable biomass. With the further increase of available burrow density, the bare patch increases and soil gradually become mesophytization, which restrained the growth of sedge plants [13] because edge plants are hygrophyte, however, in the mesophytization environment, the broad-leaved plants, such as L. virgaurea and A. lupulina, grow well because of their good reproductive and strongly adaptive ability [9], consequently, the palatable biomass decreases and the unpalatable biomass increases. 4.2. Relationship between the available burrow density and the plant diversity of alpine meadow The community structure of alpine meadow with different plant species affect where the plateau pika lives, and further regulates the population density of plateau pika to some extent, inversely, the population density of plateau pika affects on the plant species diversity of alpine meadow [14] by consuming the specific plant. Although this study generally supports the intermediate disturbance hypothesis [15], the effects of available burrow density on the richness index, evenness index and diversity index are different in the increasing process of available burrow density. The richness index and the evenness index reflect the absolute density of population and the relative the density of population in a community, and the diversity index reflects the both absolute and relative the density of population in a community [9]. The diversity index at 54 available burrow density per 625 m2 is higher than that at 34 burrow density per 625 m2 because of two reasons, firstly, the bigger pare patch encourages the competition between populations to become unsteadiness, and some plants from soil bank and some opportunistic species have chance to germinate and grow well, resulting in increasing species number in plot [16]; secondly, the increase of surface evaporation reduces the soil moisture, providing good environments for xerophyte to invade into bare patch in the alpine regions [17], and this is in accord to the result from plateau oker (Myospalax baileyi), in which grass plants invade into big molehill and increase the species number [18]. 4.3. Relationship between the available burrow density and the economic group of alpine meadow Although four economic groups are identified in the alpine meadow community, they shows the different ability of transferring primary productivity into secondary productivity [10], in which some economic groups perform higher transformation efficiency
because livestock like to feed on them. In this study, the biomass of each economic group is closely related to available burrow density of plateau pika. In weed group, some plants, including Lagotis brachystachya, Aster alpinus, Herba Taraxaci, Potentilla bifurca, P. Multifida, Polygonum sibiricum, Ajania trilobata, Leontopodium alpinum, are fed by livestock to various extents; however, others are not fed by livestock and they are L. virgaurea, Glaux maritime, Gentiana dahurica, Elsholtzia densa, Veronica polita, Saussurea japonica. The biomass of weed group is the lowest at 14 available burrow density per 625 m2 and is the highest at 54 available burrow density per 625 m2, and these implies that the modest increase of plateau pika density, increasing from 2 to 14 burrow density per 625 m2, is advantageous to improve the quality of alpine meadow by reducing the weed percentage, in which plateau pika control weeds by feeding behavior. However, the plateau pika cannot effectively control the weeds when the available burrow density is over 34 available burrow density per 625 m2, in which sedge plant with good quality is replace by weeds because the stronger activities of plateau pika changes the habitats where the sedge plants grow, such as K. humilis, K. pygmaea, and K. Capillifolia. The nutrient value and feeding value of legume group varies with the plant species. Astragalus membranaceus is high in nutrient value and feeding value, but O. coerulea is high in nutrient value and is low in feeding value, which reduces the quality of alpine meadow [10]. The biomass of legume group decreases as the available burrow density increases and disappears at 54 available burrow density per 625 m2 because plateau pika possibly feed legume plant or legume plant is not suitable for new habitats, indicating that legume group is more sensitive to environmental change than other groups. Grass group plant with high crude protein is palatable at vegetative stage, and livestock likes to feed them. The biomass of grass group increases when the available burrow density increases from 3 to 14 available burrow density per 625 m2, contributing to palatable biomass, but they are still is associate species in alpine meadow and contributing a little to the total biomass. Acknowledgments This study was supported by National Natural Science Foundation of China (31172258) and the National Science and Technology Plan of China (2009BAC53B04). References [1] X.R. Zhou, Z.G. Guo, X.H. Guo, The role of plateau pika and plateall zokor in alpine meadow, Pratacultural Science 27 (5) (2010) 28–44. [2] A.T. Smith, J.M. Foggin, The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan plateau, Animal Conservation 2 (4) (1999) 235–240. [3] H.F. Howe, J. Smallwood, Ecology of seed dispersal, Annual Reviews Ecology System 13 (1982) 201–228. [4] F.D. Sun, Z.G. Guo, Z.H. Shang, R.J. Long, Effects of density of burrowing plateau pikas (Ochotona curzoniae) on soil physical and chemical properties of alpine meadow soil, Acta Pedologica Sinica 47 (2) (2010) 378–383. [5] D.C. Andersen, J.A. Macmabon, Plant succession following the Mount St. Helens Volcanic Eruption: facilitation by a burrowing rodent, Thomomys talpoides, The American Midland Naturalist 114 (1) (1985) 62–69.
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Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
Response of alpine meadow communities to burrow density changes of plateau pika (Ochotona curzoniae) in the Qinghai-Tibet Plateau Zheng Gang Guo ⇑, Xiao Feng Li, Xing Yuan Liu, Xue Rong Zhou State Key Laboratory of Grassland Farming Systems, College of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou, China
a r t i c l e
i n f o
Keywords: Plateau pika Available burrow density Alpine meadow Qinghai-Tibetan Plateau
a b s t r a c t Plateau pika (Ochotona curzoniae) is a key component of alpine meadow ecosystem in the QinghaiTibetan Plateau, and the increase of its number leads plant components of alpine meadow ecosystem to adaptively response. A field survey was carried out to determine the response of alpine meadow community to population densities of plateau pika by using available burrow density to replace the population density of plateau pika. This study showed that the height of alpine meadow communities gradually increased, and the cover of alpine meadow communities firstly decreased, and then increased as the available burrow density increased. With the increase of available burrow density, the richness index of alpine meadow communities firstly decreased and then increased, and the evenness index of alpine meadow communities firstly increased and then decreased, however, the diversity index of alpine meadow communities firstly increased, and then decreased, finally increased. In the increasing process of available burrow density, the total plant biomass and the unpalatable plant biomass firstly decreased and then increased, and the palatable plant biomass firstly increased and then decreased, indicating that the palatable plant biomass was the highest and the unpalatable plant biomass was the lowest at 14 available burrow per 625 m2. In the economic groups of plant biomass, the weed biomass was the highest and the legume biomass was the lowest at any available burrow densities, and the grass biomass and the sedge biomass were related to available burrow densities, indicating that the sedge biomass were bigger than the grass biomass at 3 available burrow per 625 m2, inverse at 54 available burrow per 625 m2, similar between 3 and 34 available burrow per 625 m2. Accompanying by the increase of available burrow densities, the legume biomass and the sedge biomass significantly decreased (P < 0.05) and the legume became disappearance at 54 available burrow per 625 m2; the grass biomass firstly increased and then decreased, peaking at 14 available burrow per 625 m2. The weed biomass firstly decreased and then increased, and was the lowest at 14 available burrow per 625 m2. This study suggested that the responses of alpine meadow communities to population density of plateau pika at 14 available burrows per 625 m2 were more sensitive than that at other available burrow per 625 m2 from plant species diversity, biomass, height, cover and economic group. Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction The continual increase in population density of the plateau pika (Ochotona curzoniae) develops a rat trouble, which threatens the health of alpine meadow ecosystem and the development of animal husbandry economy in the Qinghai-Tibetan Plateau, but the plateau pika is a survival animal component of alpine meadow ecosystem in the process of ecosystem evolution. Previous studies have proven that the plateau pika plays the negative and positive roles in meadow alpine ecosystem, which depends on its population density [1]. The right density of plateau pika not only provides foods for endemically carnivorous mammal and raptor which lives
⇑ Corresponding author. Tel.: +86 931 8913247. E-mail address: [email protected] (Z.G. Guo).
in the Qinghai-Tibetan Plateau [2], but also acts as disperse carrier of plant seeds, which encourages some plants to expanse their distribution [1,3]. The burrow produced by plateau pika not only increases the conservation water ability of alpine meadow by enabling more rainfall to permeate into deep soil, which increases water supplies for plant growth [4], but also provides habitats, reproductive place and shelter for insects, lizard and snow finch [1]. The plateau pika has presently been considered as a keystone species in the alpine meadow ecosystem [2], and the great change of its population density generally causes the structural and functional variation of alpine meadow ecosystem. The lower density of plateau pika weakens its basically connecting link between the preceding and the following creature in the food web of alpine meadow ecosystem, however, its higher density often causes a rat trouble by competing food resources with livestock and destructing the soil structures with burrowing behavior. From self-control
1872-2032/$ - see front matter Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2011.12.002
Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49
view of ecosystem, the increase or decrease of plateau pika density arouses the changes of vegetation components in the alpine meadow ecosystem, inversely; the vegetation degradation or improvement often adjusts the plateau pika density. Therefore, the aim of plateau pika control is to keep its density into a rational density rather than never-ending decrease its density. Plant community is the core component of alpine meadow ecosystem, and its structure and components varies with the changes of plateau pika density because the activities of plateau pika increase the environmental heterogeneity [2,5] and distribution area of some spermatophyte [6], inhibits some specific plant growth due to selective intake of plateau pika [1]. The structural changes of plant community affect the habitats of plateau pika, and further affect the migration behavior of plateau pika. Previous studies have shown that the plateau pika considers the higher height and cover vegetation as a predation risk, and lives in the habitat with low vegetation height and cover, even in the habitat with bare patch [7]. Therefore, understanding the relationship between plant community and density changes of plateau pika will provide useful profile for quantifying the appropriate population density of plateau pika to control this small manual. The objective of this study is to determine the effect of density changes of plateau pika on alpine meadow communities in the Qinghai-Tibet Plateau by using available burrow density substituting for plateau pika density.
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recorded by closing burrow exit for three days in May, 2009, and the distance between plots was over 50 m. According to available burrow number in plot, the plots was divided into four categories, in which 3(3 ± 1), 14(14 ± 2), 34(34 ± 3), and 54(54 ± 4) available burrow density per 625 m2 were finally selected to investigate the response of alpine meadow communities to available burrow densities of plateau pika, and each category was three plot as replicates. 2.3. Field survey and sampling The field survey was conducted from late July to early August in 2009. In each plot, five subplots with the size of 1 m 1 m were designed with ‘‘W’’ pattern distribution to collect quantitative data on the vegetation and distance between subplots was over 10 m. The total number of subplots was 60. In each subplot, present species number, total biomass and every species biomass (g), vegetation height and every species height (cm), total cover and every species cover (%) were recorded. The total foliage cover was measured by using 100 points (1 mm wire). Vegetation height was measured by lowering a perforated foam disc (diameter 0.1 m, weight 7 g) onto the vegetation along a gauged stick. Aboveground materials of all plants rooted in each subplot were collected by single species, and carried back, and then dried at 80 °C for 24 h and weighed in the laboratory. Subplot data within each plot were pooled. 2.4. Data analysis
2. Methods and materials 2.1. Study area The study was carried out in the Dawu town of Maqin County, Qinghai Province (32°310 –35°31, 96°540 –101°510 ). The study area locates in the Yellow River source area of Qinghai-Tibetan Plateau with the average elevation from 3874 m to 3780 m. The annual mean precipitation is 528.5 mm, mainly taking place during the period June to September, and the annual evaporation is 2470 mm. The mean temperature is -3.9 °C without free frost period. The climate in this area is plateau continental climate, in which spring, summer, autumn and winter is not identified, and the climate is divided into short warm season (from June to September) and long cool season (from October to May). The accumulative temperature with P5 °C is 850 °C and the period of plant growth is only 156 d. The soil is alpine meadow soil and alpine bush meadow soil with 30–50 cm thick [4], and their parent materials are chiefly residual deposits with coarse texture, consisting mostly of sand. Original vegetation is alpine meadow, which is dominated by Kobresia humilis with the main associate plant species of Kobresia pygmaea, Kobresia capillifolia, Aconitum szechenyianum, Stekkera chamaejasme, Ligularia virgaurea, Oxytropis coerulea, Elymus nutans, Poa annua, Stipa aliena, Leontopodium leontonpodioides, Ajuga lupulina, Artemisia nanschanica and Potentilla sp. 2.2. Experimental design A field survey was carried out on the cool season rangeland to avoid the effect of grazing on alpine communities in the process of survey, in which the yak and Tibetan sheep was grazed from middle October to early April, and rangeland during warm season is close grazing. It is difficult to determine plateau pika density by recording its number due to its family life pattern, therefore, the available burrow density of plateau pika was used to substitute for its own density. The higher available burrow density meant the higher plateau pika density [8]. Forty survey plots with the size of 25 m 25 m (625 m2) was randomly selected on the similar meadow flat and the available burrow density in each plot was
Importance value of species was calculated with the equation, IV = (relative height + relative cover + relative biomass)/3, and it was used to determine the dominant species and associate species. Three indices were chosen for estimation of a diversity [9], (1) the richness index (S) is represented by number of species recorded in each subplot; (2) the diversity index was measured P by the Shannon–Wiener’s index of diversity, H ¼ ni¼1 Pi LnPi i; and (3) the evenness index was measured by the Pielou’s index of evenness, J sw ¼ H=LnS, where Pi ¼ N i =N; Ni is the importance value of individual species i; N is the total individuals of all species present; S is number of vascular species present. Based on principle of grassland utilization, the plant in subplot was divided into four economic groups, including grass group, sedge group, legume group, and weed group [10]. Differences in plant species diversity, cover, biomass, and soil parameters among alpine meadows of four available burrow densities were analyzed by using one-way ANOVA. 3. Results 3.1. Effect of available burrow densities on component and vertical structure of plant communities The number of plant species ranged from 43 to 32 in the subplot, and firstly increased and then decreased as the available burrow density increased (Table 1). Although the dominant species always was K. humilis, the associate species obviously changed with the increase of the available burrow density, indicating that A. szechenyianum at 3 available burrow density per 625 m2 was replaced by S. chamaejasma at 14 available burrow density per 625 m2, and replaced by L. virgaurea and O. coerulea at 34 and 54 available burrow density per 625 m2, respectively. The change of associate species in plant communities resulted in difference of family and genus. The number of plant species and genus in the subplots firstly decreased and then increased, and was the lowest at 34 available burrow density per 625 m2; however, the number of family in the subplots firstly increased and then decreased, peaking at 14 available burrow density per 625 m2.
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Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49
Table 1 Effect of available burrow densities of plateau pika on community structure of alpine meadow. Burrow densities (number/ 625 m2)
Dominant species
Associate species
Species number Familia
Genus
Species
3 14 34 54
Kobresia Kobresia Kobresia Kobresia
Aconitum szechenyianum, Kobresia capillifolia Stellera chamaejasma, Leontopodium alpinum Ligularia virgaurea, Artemisia nanschanica Oxytropis coerulea, Ajuga lupulina
16 20 16 16
38 33 29 30
43 37 32 35
humilis humilis humilis humilis
The available burrow density greatly affected the vertical structure of plant communities. The plant communities at 3 available burrow density per 625 m2 were double layers, in which A. szechenyianum occupied the upper layer and the plants from sedge family grew at low layer. At 14 available burrow density per 625 m2 conditions, the upper layer was occupied by grass and S. chamaejasma and the low layer was took up by plant from sedge genus and low weeds. The vertical structure of plant communities varied with the growing season of main associate plants when the available burrow density was over or equal to 34 burrow density per 625 m2, indicating that the plant communities were single layer when L. virgaurea and O. coerulea was vegetative growth stage and they were double layers when L. virgaurea and O. coerulea entered into reproductive growth stage. 3.2. Effect of available burrow densities on height and cover of plant communities The height of plant communities decreased as the available burrow density increased (Fig. 1A), indicating that the height of plant communities at 3 available burrow density per 625 m2 was significantly bigger than that at 34 and 54 available burrow density per 625 m2 (P < 0.05). The cover of plant communities firstly decreased and then increased with the increase of available burrow density
A
Vertical structure
2 2 1or 2 1or 2
(Fig. 1B), and it was the lowest and was over or equal to 80% at 14 available burrow density per 625 m2. 3.3. Effect of available burrow densities on species diversity of plant communities With the increase of available burrow density, the richness index of plant communities firstly decreased and then increased (Fig. 2A), indicating that the richness index at 34 available burrow density per 625 m2 was the lowest and significantly lower than that at other burrow densities per 625 m2 (P < 0.05). The evenness index of plant communities firstly increased and then decreased as the available burrow density increased (Fig. 2B), and it peaked at 14 available burrow density per 625 m2 and was significantly bigger than that at 3 and 54 available burrow density per 625 m2. The diversity index of plant communities was not different between 14 burrow number per 625 m2 and 54 available burrow number per 625 m2, and they were significantly bigger than those at 34 and 3 available burrow number per 625 m2 (Fig. 2C). 3.4. Effect of available burrow densities on biomass of plant communities The total plant biomass firstly decreased and then increased as the available burrow density increased (Fig. 3A), and was the lowest at 14 available burrow densities per 625 m2. The palatable plant biomass was not consistent with the unpalatable plant biomass (Fig. 3B). The palatable plant biomass increased from 3 available burrow density per 625 m2 to 14 available burrow density per 625 m2 and decreased when the available burrow density per 625 m2 was over 14, and the unpalatable plant biomass firstly decreased and then increased with the increase of available burrow density, and was the lowest at 14 available burrow density per 625 m2, and these implied that the increase of available burrow density changed the total biomass and palatable biomass, in which 14 available burrow density per 625 m2 was points of inflection point. 3.5. Effect of available burrow densities on economic groups of plant communities
B
Fig. 1. Effect of available burrow densities of plateau pika on height (A) and cover (B) of alpine meadow.
The biomass of weed group accounted for the largest percentage of the total plant biomass at four available burrow densities (Table 2), mainly consisting of Delphinium grandiflorum, Ajania purpurea, Pedicularis kansuensis, A. szechenyianum, L. virgaurea; however, the biomass of legume group mainly deriving Astragalus membranaceus and Gueldenstaedtia verna was the lowest. The percentage of grass and sedge group biomass in the total plant biomass varied with the increase of available burrow density. The biomass of sedge group was bigger than the biomass of grass group at 3 available burrow density per 625 m2, and was lower than the biomass of grass group at 14 available burrow density per 625 m2, and the biomass of grass and sedge group was similar when available burrow density was over or equal to 34 available burrow density per 625 m2. The biomass of legume group significantly decreased as the available burrow density increased
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Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49
A
30
a
A
b
a
180
20 15 10
ab
b
b
150
Total biomass (g/m2)
25
Richness index
ab
ab
120 90 60 30
5 0 3
0 3
14
34
54
14
34
54
Available burrow densities (number/625m2)
Available burrow densities (number/625m2)
Evenness index
1
160
Palatable
140
b
a
ab
b
0.8 0.6 0.4
Biomass (g/m2)
B
B
1.2
a
a
a
Unpalatable
120
b
100 80 60
a
b
c
40
c
20 0 3
0.2
14
34
54
Available burrow densities (number/625m2) 0 3
14
34
54
Available burrow densities (number/625m2)
C
3.5 3
Diversity index
Fig. 3. Effect of available burrow densities of plateau pika on the total biomass (A), and palatable and unpalatable biomass (B) of alpine meadow community (The same bar with the different a, b and c means significant difference at 0.05 level).
b
a
3
14
b
a
2.5 2 1.5 1 0.5 0
34
54
Available burrow densities (number/625m2) Fig. 2. Effect of available burrow densities of plateau pika on the richness index (A), evenness index (B), and diversity index (C) of alpine meadow community.
(P < 0.05) and disappeared at 54 available burrow density per 625 m2. The biomass of weed group firstly decreased and then increased with the increase of available burrow density, and was the lowest at 14 available burrow density per 625 m2. This study showed that the most sensitive response of weed, sedge, grass group to available burrow density was 14 available burrow densities per 625 m2. 4. Discussions 4.1. Relationship between the available burrow density and the structure and productivity of alpine meadow The activities of plateau pika redistribute the light energy and water resources to various extent in the land surface and soil when
the plateau pika enters into slightly degraded alpine meadow, which affects the plant growth consisting of plant communities by directly or indirectly ways [7], sometimes, developing a shortterm stability habitat. This habitat often varies with the increase of plateau pika density. This study suggests that the available burrow density affect the primary productivity of alpine meadow by changing the vertical structure, plant species number, height, cover and biomass. The disturbance of plateau pika activities on alpine meadow is very weak at 3 available burrow density per 625 m2; consequently, the alpine meadow maintains its own features and productivity. At 14 available burrow density per 625 m2, the vegetation cover decreases because the more plant was grazed and buried by plateau feeding and burrowing behavior. With the further increase of available burrow density, the bare patch increases [8], and this provides invasion changes for opportunistic species, especially broad-leaves plant, resulting in increasing the vegetation cover. The plateau pika affects the vertical structure of alpine meadow community by causing the replacement of associate species, and the growth stages of these associate species regulates the vertical structure. At 34 available burrow density per 625 m2, the vertical structure of alpine meadow community changed from single layer into double layers when L. virgaurea grows from vegetative stage with low height to reproductive stage with the high height, and this implies that the influence of plateau pika on the vertical structure of alpine meadow community is related to sample time because the height of broad-leaved plant was different between vegetative stage and reproductive stage [11]. As the available burrow density increases, the total biomass and unpalatable biomass firstly decreases and then increases, and the palatable biomass shows a inversely trend, at the same time, the biomass of weed group accounts for the biggest percentage of the total biomass, and these imply that the total biomass of alpine meadow is determined by weeds not palatable plant and the
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Z.G. Guo et al. / Acta Ecologica Sinica 32 (2012) 44–49 Table 2 Effect of available burrow densities of plateau pika on economic groups of alpine meadow (g/m2). Burrow densities (number/ 625 m2)
Grass
Sedge
Legume
Weed
3 14 34 54
11.75 ± 1.23c 30.26 ± 2.34a 12.39 ± 1.98c 16.75 ± 2.01bc
46.09 ± 3.21a 28.12 ± 2.41b 13.67 ± 1.89c 11.94 ± 2.12c
1.88 ± 0.23a 1.52 ± 0.12b 0.99 ± 0.08c 0
104.99 ± 10.36b 81.02 ± 4.52c 121.51 ± 9.56a 124.43 ± 11.23a
Note: The data means the average value ± SE, and the data with the same letter in a column was not significantly different at 0.05 level.
activities of rational plateau pika improve the quality of alpine meadow [10] by increasing the palatable biomass. Alpine meadow maintains its own competition pattern of plant populations because the plateau pika has limited influence over alpine meadow when its density is low [12], in which A. szechenyianum is mainly associate species with high height and rich leaves and stems. The increase of available burrow density encourages S. chamaejasma and L. alpinum with low height to replace the A. szechenyianum and to become the mainly associate species, which provides the good light for palatable sedge plant growing at the low layer, resulting in increasing the palatable biomass. With the further increase of available burrow density, the bare patch increases and soil gradually become mesophytization, which restrained the growth of sedge plants [13] because edge plants are hygrophyte, however, in the mesophytization environment, the broad-leaved plants, such as L. virgaurea and A. lupulina, grow well because of their good reproductive and strongly adaptive ability [9], consequently, the palatable biomass decreases and the unpalatable biomass increases. 4.2. Relationship between the available burrow density and the plant diversity of alpine meadow The community structure of alpine meadow with different plant species affect where the plateau pika lives, and further regulates the population density of plateau pika to some extent, inversely, the population density of plateau pika affects on the plant species diversity of alpine meadow [14] by consuming the specific plant. Although this study generally supports the intermediate disturbance hypothesis [15], the effects of available burrow density on the richness index, evenness index and diversity index are different in the increasing process of available burrow density. The richness index and the evenness index reflect the absolute density of population and the relative the density of population in a community, and the diversity index reflects the both absolute and relative the density of population in a community [9]. The diversity index at 54 available burrow density per 625 m2 is higher than that at 34 burrow density per 625 m2 because of two reasons, firstly, the bigger pare patch encourages the competition between populations to become unsteadiness, and some plants from soil bank and some opportunistic species have chance to germinate and grow well, resulting in increasing species number in plot [16]; secondly, the increase of surface evaporation reduces the soil moisture, providing good environments for xerophyte to invade into bare patch in the alpine regions [17], and this is in accord to the result from plateau oker (Myospalax baileyi), in which grass plants invade into big molehill and increase the species number [18]. 4.3. Relationship between the available burrow density and the economic group of alpine meadow Although four economic groups are identified in the alpine meadow community, they shows the different ability of transferring primary productivity into secondary productivity [10], in which some economic groups perform higher transformation efficiency
because livestock like to feed on them. In this study, the biomass of each economic group is closely related to available burrow density of plateau pika. In weed group, some plants, including Lagotis brachystachya, Aster alpinus, Herba Taraxaci, Potentilla bifurca, P. Multifida, Polygonum sibiricum, Ajania trilobata, Leontopodium alpinum, are fed by livestock to various extents; however, others are not fed by livestock and they are L. virgaurea, Glaux maritime, Gentiana dahurica, Elsholtzia densa, Veronica polita, Saussurea japonica. The biomass of weed group is the lowest at 14 available burrow density per 625 m2 and is the highest at 54 available burrow density per 625 m2, and these implies that the modest increase of plateau pika density, increasing from 2 to 14 burrow density per 625 m2, is advantageous to improve the quality of alpine meadow by reducing the weed percentage, in which plateau pika control weeds by feeding behavior. However, the plateau pika cannot effectively control the weeds when the available burrow density is over 34 available burrow density per 625 m2, in which sedge plant with good quality is replace by weeds because the stronger activities of plateau pika changes the habitats where the sedge plants grow, such as K. humilis, K. pygmaea, and K. Capillifolia. The nutrient value and feeding value of legume group varies with the plant species. Astragalus membranaceus is high in nutrient value and feeding value, but O. coerulea is high in nutrient value and is low in feeding value, which reduces the quality of alpine meadow [10]. The biomass of legume group decreases as the available burrow density increases and disappears at 54 available burrow density per 625 m2 because plateau pika possibly feed legume plant or legume plant is not suitable for new habitats, indicating that legume group is more sensitive to environmental change than other groups. Grass group plant with high crude protein is palatable at vegetative stage, and livestock likes to feed them. The biomass of grass group increases when the available burrow density increases from 3 to 14 available burrow density per 625 m2, contributing to palatable biomass, but they are still is associate species in alpine meadow and contributing a little to the total biomass. Acknowledgments This study was supported by National Natural Science Foundation of China (31172258) and the National Science and Technology Plan of China (2009BAC53B04). References [1] X.R. Zhou, Z.G. Guo, X.H. Guo, The role of plateau pika and plateall zokor in alpine meadow, Pratacultural Science 27 (5) (2010) 28–44. [2] A.T. Smith, J.M. Foggin, The plateau pika (Ochotona curzoniae) is a keystone species for biodiversity on the Tibetan plateau, Animal Conservation 2 (4) (1999) 235–240. [3] H.F. Howe, J. Smallwood, Ecology of seed dispersal, Annual Reviews Ecology System 13 (1982) 201–228. [4] F.D. Sun, Z.G. Guo, Z.H. Shang, R.J. Long, Effects of density of burrowing plateau pikas (Ochotona curzoniae) on soil physical and chemical properties of alpine meadow soil, Acta Pedologica Sinica 47 (2) (2010) 378–383. [5] D.C. Andersen, J.A. Macmabon, Plant succession following the Mount St. Helens Volcanic Eruption: facilitation by a burrowing rodent, Thomomys talpoides, The American Midland Naturalist 114 (1) (1985) 62–69.
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