Effect of plant species loss on grassland caterpillar in alpine meadows

doi:10.17520/biods.2022069

Abstract

Abstract:

Aims: Plant diversity plays a crucial role in regulating food web dynamics and ecosystem functioning. Existing studies have documented significant impact on large herbivores and ecosystem functioning from loss in plant species diversity. Yet, little is known about effect of plant diversity loss on small herbivores and its functional consequence on food web dynamics, ecosystem functioning and ecosystem service, due to difficulty in distinguishing the role of plant diversity from larger fluctuations of small herbivore populations under the confounding effect of multiple ecological factors and demographic stochasticity.

Methods: Based on our long-term experiment of plant species removal in an alpine meadow on the Tibetan Plateau, we repeatedly measured the number of grassland caterpillar (Gynaephora alpherakiif) in each plot (i.e. density) in July and August over five years (2016-2020). We examined the effect of plant species removal on caterpillar population by associating changes in caterpillar counts with a shift in plant community attributes following plant removal and using a set of generalized linear mixed models.

Results: Plant removal induced a difference in the plant community, which significantly and consistently influenced the caterpillar counts over years and months independent of the observed variation in caterpillar counts accounted for by the difference in years and observational times within each month. Comparing the caterpillar counts in plots without removing plant species, (i) the caterpillar counts decreased in plots subjected to removal of dominant species (Kobresia capillifolia) in both July and August across five years, and increased in plots subjected to removal of forbs species in August of 2016 and 2019, and (ii) the caterpillar counts tended to increase in plots subjected to removal of legume species but only significantly in few cases, and did not significantly differ with plots subjected to removal of partial species (accounting for 20% aboveground biomass) of each functional groups. Further analysis showed that neither total aboveground biomass nor plant species richness and total individual numbers was significantly correlated with the caterpillar counts. The variation in caterpillar counts was associated positively with aboveground biomass of sedges and grasses as well as grass species richness, but negatively with the amount of forbs and legumes. The structural equation model further revealed that the removal of Kobresiaand grass species affected caterpillar counts through decreasing aboveground biomass of graminoids, but increasing graminoids following removal of forb and legume species promoted the density of caterpillars.

Conclusion: Based on field observations on the grassland caterpillar populations in plots subjected to different removal protocols, our study provides robust evidence that the decline in relative abundance of graminoids significantly reduced the fitness of caterpillars, and thus potentially impacts grassland functioning and ecosystem service. This study also suggests that future research on biodiversity effects and biological control of pests needs to pay more attention to the effects of plant functional diversity and demographic stochasticity on small herbivores.

Key words: species diversity, community assembly, demographic stochasticity, repeated measurement, functional group, functional traits

Yongqingcuomu , Xinqiang Xi, Kechang Niu. Effect of plant species loss on grassland caterpillar in alpine meadows[J]. Biodiv Sci, 2022, 30(11): 22069.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2022069

https://www.biodiversity-science.net/EN/Y2022/V30/I11/22069

Figures/Tables 5

Table 1 Effect of year, month, repeated measurement and plant species removal on counts of grassland caterpillar assessed by generalized linear mixed models (GLMM). The tabular (estimated) slopes (mean ± SD) from GLMM measured the effect of fixed factors on caterpillar counts, with direction, strength and significance of the effects indicated by + (increased) or - (decreased), absolute size of value and * (* P < 0.05, ** P < 0.01), respectively. Ksp: Removal of Kobresia capillifoli; Gsp: Removal of grass species; Fsp: Removal of forb species; Lsp: Removal of legume species; Psp: Removal of partial species for each functional group.

影响效应 Effect size
年际影响 Effect of years (变异解释 Variability = 10.7%, F = 114.6^**, df = 4)
2017 vs. 2016	0.28 ± 0.03^**
2018 vs. 2016	0.12 ± 0.03^**
2019 vs. 2016	-0.54 ± 0.04^**
2020 vs. 2016	-0.44 ± 0.04^**
月份影响 Effect of months (变异解释 Variability = 1.9%, F = 16.3^**, df = 5)
8月vs. 7月August vs. July	-0.04 ± 0.02
重复测量影响 Effect of repeated measurement (变异解释 Variability = 40.8%, F = 48.8^**, df = 36)
第一次 1st vs. 0th observation	-0.36 ± 0.03^**
第二次 2nd vs. 0th observation	-0.70 ± 0.03^**
第三次 3rd vs. 0th observation	-0.84 ± 0.03^**
第四次 4th vs. 0th observation	-1.2 ± 0.04^**
植物剔除处理影响 Effect of plant removal (变异解释 Variability = 8.3%, F =1.5^**, df = 230)
剔除优势嵩草vs.对照 K_sp vs. CK	-0.29 ± 0.04^**
剔除禾草物种vs.对照 G_sp vs. CK	-0.19 ± 0.04^**
剔除杂类草物种vs.对照 F_sp vs. CK	0.12 ± 0.03^**
剔除豆科物种vs.对照 L_sp vs. CK	0.06 ± 0.03
各功能群部分物种剔除vs.对照 P_sp vs. CK	-0.02 ± 0.03
残差 Residuals (变异解释 Variability = 38.4%, df = 1,653)

Fig. 1 Effect of plant species removal on numbers of grassland caterpillar in each year and month in a Tibetan alpine meadow assessed by generalized linear mixed models (GLMM). Comparing to caterpillar counts in plots (CK) without removing plant species (a), the effect of plant species removal in each year and month on the caterpillar counts indicated by values and 95% confidence interval (CI) of estimated slopes from GLMM, with significant (95% CI not overlap with zero, * P < 0.05, ** P < 0.01) positive (blue) and negative (red) effect highlighted by colored values with * and CI of the estimated slopes, and values without * and CI (overlap with zero) indicated non-significant difference between CK and treatment of plant species removal. Ksp, Gsp, Fsp, Psp, CK and Lsp see Table 1.

Table 2 Effect of year and plant species removal on plant community attributes assessed by linear mixed models (GLMM). The tabular values from GLMM measured the effect of fixed factors (year and treatment of plant species removal) on plant community attributes, including accounted variability (%), significance test of difference (F-value with P-value), and estimated slopes (mean ± SD) that indicate direction (+ increased, - decreased) and strength (absolute size of value) of effect of difference in year (each year vs. 2016) or in plant species removal (each treatment vs. CK plots without removing any species) on plant community attributes, with significance highlighted by bold (P < 0.1) and * (* P < 0.05, ** P < 0.01). Ksp, Gsp, Fsp, Psp, CK and Lsp see Table 1.

	物种丰富度 Species richness	总个体数 Total individuals	总生物量 Total biomass	各功能群生物量 Biomass for each functional group
	物种丰富度 Species richness	总个体数 Total individuals	总生物量 Total biomass	莎草 Sedges	禾草 Grasses	杂类草 Forbs	豆科 Legumes
年际影响 Effect of years
变异解释 Variability (%)	34.5%	49.7%	79.9%	50.9%	20.2%	46.8%	26.8%
F	139.8^**	127.7^**	455.6^**	193.1^**	75.7^**	226.9^**	57.9^**
自由度 df	3	3	3	3	3	3	3
影响效应 Effect size (与2016年比, 各年的影响以斜率均值 ± 标准差衡量 Effect size of year vs. 2016 was measured by mean ± SD of slopes)
2017	0.06 ± 0.02	0.26 ± 0.01^**	-81.5 ± 2.7^**	-25.7 ± 1.5^**	-2.9 ± 1.5	-45.6 ± 2.5^**	-7.1 ± 0.6^**
2019	0.29 ± 0.03^**	0.66 ± 0.01^**	-51.5 ± 2.7^**	-11.8 ± 1.4^**	-1.7 ± 1.5	-35.9 ± 2.5^**	-4.6 ± 0.6^**
2020	0.30 ± 0.03^**	0.51 ± 0.01^**	-89.8 ± 2.7^**	-25.8 ± 1.4^**	-17 ± 1.5^**	-44.9 ± 2.5^**	-4.4 ± 0.6^**
物种剔除影响 Effect of species removal
变异解释 Variability (%)	39.8%	9.7%	1.90%	22.3%	52.6%	32.1%	28.3%
F	24.1^**	3.7^**	1.62^*	12.7^**	29.6	23.4^**	9.2^**
自由度 df	20	20	20	20	20	20	20
影响效应 Effect size (与对照比, 各处理的影响以斜率均值 ± 标准差度量 Effect size of treatment vs. CK was measured by mean ± SD of slopes)
剔除优势嵩草 K_sp	-0.05 ± 0.03	-0.11 ± 0.01^**	-5.4 ± 3.3	-11.4 ± 1.8^**	-1.7 ± 1.8	-4.8 ± 3.1	-0.5 ± 0.7
剔除禾草物种 G_sp	-0.20 ± 0.03^**	-0.11 ± 0.01^**	-7.70 ± 3.3^*	-0.36 ± 1.8	-14.4 ± 1.9^**	7.8 ± 3.1^*	-0.5 ± 0.7
剔除杂类草物种 F_sp	-0.45 ± 0.04^**	-0.30 ± 0.01^**	-8.0 ± 3.3^*	6.0 ± 1.8^**	19.2 ± 1.9^**	-31.1 ± 3.1^**	5.7 ± 0.7^**
剔除豆科物种 L_sp	-0.07 ± 0.03^*	-0.09 ± 0.01^**	-7.6 ± 3.3^*	-0.42 ± 1.8	-0.5 ± 1.8	-4.7 ± 3.1	-2.3 ± 0.8^**
各功能群部分物种剔除 P_sp	-0.11 ± 0.03^**	-0.19 ± 0.01^**	-3.7 ± 3.3	-3.8 ± 1.7^*	-2.7 ± 1.8	-1.7 ± 3.1	1.1 ± 0.7
残差 Residuals
变异解释 Variability (%)	25.7%	40.5%	18.2%	26.9%	27.2%	21.2%	45.0%
自由度 df	312	312	312	306	306	308	292

	物种丰富度 Species richness	总个体数 Total individuals	总生物量 Total biomass	各功能群生物量 Biomass for each functional group
	物种丰富度 Species richness	总个体数 Total individuals	总生物量 Total biomass	莎草 Sedges	禾草 Grasses	杂类草 Forbs	豆科 Legumes
年际影响 Effect of years
变异解释 Variability (%)	34.5%	49.7%	79.9%	50.9%	20.2%	46.8%	26.8%
F	139.8^**	127.7^**	455.6^**	193.1^**	75.7^**	226.9^**	57.9^**
自由度 df	3	3	3	3	3	3	3
影响效应 Effect size (与2016年比, 各年的影响以斜率均值 ± 标准差衡量 Effect size of year vs. 2016 was measured by mean ± SD of slopes)
2017	0.06 ± 0.02	0.26 ± 0.01^**	-81.5 ± 2.7^**	-25.7 ± 1.5^**	-2.9 ± 1.5	-45.6 ± 2.5^**	-7.1 ± 0.6^**
2019	0.29 ± 0.03^**	0.66 ± 0.01^**	-51.5 ± 2.7^**	-11.8 ± 1.4^**	-1.7 ± 1.5	-35.9 ± 2.5^**	-4.6 ± 0.6^**
2020	0.30 ± 0.03^**	0.51 ± 0.01^**	-89.8 ± 2.7^**	-25.8 ± 1.4^**	-17 ± 1.5^**	-44.9 ± 2.5^**	-4.4 ± 0.6^**
物种剔除影响 Effect of species removal
变异解释 Variability (%)	39.8%	9.7%	1.90%	22.3%	52.6%	32.1%	28.3%
F	24.1^**	3.7^**	1.62^*	12.7^**	29.6	23.4^**	9.2^**
自由度 df	20	20	20	20	20	20	20
影响效应 Effect size (与对照比, 各处理的影响以斜率均值 ± 标准差度量 Effect size of treatment vs. CK was measured by mean ± SD of slopes)
剔除优势嵩草 K_sp	-0.05 ± 0.03	-0.11 ± 0.01^**	-5.4 ± 3.3	-11.4 ± 1.8^**	-1.7 ± 1.8	-4.8 ± 3.1	-0.5 ± 0.7
剔除禾草物种 G_sp	-0.20 ± 0.03^**	-0.11 ± 0.01^**	-7.70 ± 3.3^*	-0.36 ± 1.8	-14.4 ± 1.9^**	7.8 ± 3.1^*	-0.5 ± 0.7
剔除杂类草物种 F_sp	-0.45 ± 0.04^**	-0.30 ± 0.01^**	-8.0 ± 3.3^*	6.0 ± 1.8^**	19.2 ± 1.9^**	-31.1 ± 3.1^**	5.7 ± 0.7^**
剔除豆科物种 L_sp	-0.07 ± 0.03^*	-0.09 ± 0.01^**	-7.6 ± 3.3^*	-0.42 ± 1.8	-0.5 ± 1.8	-4.7 ± 3.1	-2.3 ± 0.8^**
各功能群部分物种剔除 P_sp	-0.11 ± 0.03^**	-0.19 ± 0.01^**	-3.7 ± 3.3	-3.8 ± 1.7^*	-2.7 ± 1.8	-1.7 ± 3.1	1.1 ± 0.7
残差 Residuals
变异解释 Variability (%)	25.7%	40.5%	18.2%	26.9%	27.2%	21.2%	45.0%
自由度 df	312	312	312	306	306	308	292

Fig. 2 Effect of plant community attributes on numbers of grassland caterpillar in a Tibetan alpine meadow assessed by generalized linear mixed models (GLMM). Using difference in years and month as random factors, the values and 95% confidence interval (CI) of estimated slopes from GLMM measured the effect of whole community attributes (aboveground biomass, individual numbers and species numbers) on caterpillar counts (a-e), aboveground biomass (f-j), individual numbers (k-o), and species numbers (p-t) of each functional groups on the caterpillar counts, with significant positive (blue) and negative (red) effect highlighted by values with * and CI (not overlap with zero) of the estimated slopes (* P < 0.05, ** P < 0.01, no * but bolded values indicates 0.05 < P < 0.1), and the values without * and CI (not overlap zero) indicated non-significant effect.

Fig. 3 Structural equation model (SEM) revealed the effect of plant species removal in the alpine meadow on caterpillar counts mostly via change in attribute and structure of plant communities. Using difference in year and month as random factors, the estimated slopes in SEM measured effect of plant species removal on plant community as well as plant community on caterpillar counts, with blue and red single-arrowed lines accompanying values with * indicate significant (* P < 0.05, ** P < 0.01, no * 0.05 < P < 0.1) positive and negative effect (the width of lines corresponding to the values that indicate strength of the effect), respectively; gray double-arrowed lines for correlations between variables of plant community. R2c indicates explanation of plant removal treatment on variables of plant community and later to Caterpillar numbers. Global goodness-of-fit: Fisher’s C = 16.2, P = 0.09, df = 10.

References 53

[1]	Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48.
[2]	Cao H, Zhu WY, Zhao XQ (2016) Effects of warming and grazing on growth and development of the grassland caterpillar (Gynaephora menyuanensis). Acta Prataculturae Sinica, 25, 268-272. (in Chinese with English abstract)
	[曹慧, 朱文琰, 赵新全 (2016) 试验增温和放牧对门源草原毛虫生长发育的影响. 草业学报, 25, 268-272.]
[3]	Cease AJ, Elser JJ, Ford CF, Hao SG, Kang L, Harrison JF (2012) Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content. Science, 335, 467-469. DOI PMID
[4]	Chen KL, Yu XC, Yao BQ, Ma Z, Wang WY, Wang HC, Zhou HK, Zhao XQ (2016) Spatial distribution of Gynaephora menyuanensis under different grazing intensities in alpine meadow. Acta Agrestia Sinica, 24, 191-197. (in Chinese with English abstract)
	[陈珂璐, 余欣超, 姚步青, 马真, 王文颖, 王慧春, 周华坤, 赵新全 (2016) 不同放牧强度下门源草原毛虫在高寒草甸上的空间分布. 草地学报, 24, 191-197.] DOI
[5]	Corlett RT (2016) Plant diversity in a changing world: Status, trends, and conservation needs. Plant Diversity, 38, 10-16. DOI PMID
[6]	Delignette-Muller ML, Dutang C (2015) fitdistrplus: An R package for fitting distributions. Journal of Statistical Software, 64(4), 1-34.
[7]	Díaz S, Settele J, Brondízio ES, Ngo HT, Agard J, Arneth A, Balvanera P, Brauman KA, Butchart SHM, Chan KMA, Garibaldi LA, Ichii K, Liu JG, Subramanian SM, Midgley GF, Miloslavich P, Molnár Z, Obura D, Pfaff A, Polasky S, Purvis A, Razzaque J, Reyers B, Chowdhury RR, Shin YJ, Visseren-Hamakers I, Willis KJ, Zayas CN (2019) Pervasive human-driven decline of life on Earth points to the need for transformative change. Science, 366, eaax3100.
[8]	Díaz S, Symstad AJ, Chapin FS III, Wardle DA, Huenneke LF (2003) Functional diversity revealed by removal experiments. Trends in Ecology & Evolution, 18, 140-146.
[9]	Dong SK, Shang ZH, Gao JX, Boone RB (2020) Enhancing sustainability of grassland ecosystems through ecological restoration and grazing management in an era of climate change on Qinghai-Tibetan Plateau. Agriculture, Ecosystems & Environment, 287, 106684.
[10]	Duffy JE, Godwin CM, Cardinale BJ (2017) Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature, 549, 261-264.
[11]	Gao Q, Yang ZL (2010) Ectomycorrhizal fungi associated with two species of Kobresia in an alpine meadow in the eastern Himalaya. Mycorrhiza, 20, 281-287.
[12]	Gu HJ, Wang H, Shangguan ZJ, Shi HJ, Zhu JX, He JS (2022) Effects of nitrogen addition on the population density of Gynaephora menyuanensis in Tibetan alpine grassland. Acta Ecologica Sinica, 42, 1958-1967 (in Chinese with English abstract)
	[顾慧洁, 汪浩, 上官子健, 石慧瑾, 朱剑霄, 贺金生 (2022) 外源氮添加对高寒草地门源草原毛虫种群密度的影响. 生态学报, 42, 1958-1967.]
[13]	Hair JF, Black WC, Babin BJ, Anderson RE (2010) Multivariate Data Analysis, 7th edn. Prentice Hall, Englewood Cliffs, NJ.
[14]	He XD, Wang WJ (2003) Preliminary study on distribution region and damage grades of grassland caterpillar in Qinghai. Pratacultural Science, 20(8), 45-48. (in Chinese)
	[何孝德, 王薇娟 (2003) 青海省草原毛虫分布区域及为害等级划分初探. 草业科学, 20(8), 45-48.]
[15]	Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Högberg P, Huss-Danell K, Joshi J, Jumpponen A, Körner C, Leadley PW, Loreau M, Minns A, Mulder CP, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze ED, Siamantziouras ASD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science, 286, 1123-1127. DOI PMID
[16]	Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature, 486, 105-108.
[17]	Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature, 477, 199-202.
[18]	Jiang L, Hu J, Yang ZA, Zhan W, Zhao C, Zhu D, He YX, Chen H, Peng CH (2021) Effects of plant functional group removal on community structure, diversity and production in alpine meadow. Acta Ecologica Sinica, 41, 1402-1411. (in Chinese with English abstract)
	[姜林, 胡骥, 杨振安, 詹伟, 赵川, 朱单, 何奕忻, 陈槐, 彭长辉 (2021) 植物功能群去除对高寒草甸群落结构、多样性及生产力的影响. 生态学报, 41, 1402-1411.]
[19]	Kang L, Han XG, Zhang ZB, Sun OJ (2007) Grassland ecosystems in China: Review of current knowledge and research advancement. Philosophical Transactions of the Royal Society B: Biological Sciences, 362, 997-1008.
[20]	Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Danell K (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia, 125, 271-282. DOI PMID
[21]	Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods in Ecology and Evolution, 7, 573-579.
[22]	Liu YZ, Reich PB, Li GY, Sun SC (2011) Shifting phenology and abundance under experimental warming alters trophic relationships and plant reproductive capacity. Ecology, 92, 1201-1207. PMID
[23]	Lüdecke D, Schwemmer C (2017) sjPlot: Data Visualization for Statistics in Social Science. Version 2.4.0. https://CRAN. R-project.org/package=sjPlot.
[24]	Ma PJ, Li YJ, Pan DF, Chen BJ, Li XC, Wang DL (2017) Effect of grassland caterpillar on the characteristics of the vegetation of Kobresia pygmaea alpine grassland under the interference of the yak grazing. Pratacultural Science, 34, 698-705. (in Chinese with English abstract)
	[马培杰, 李亚娇, 潘多锋, 陈本建, 李心诚, 王德利 (2017) 牦牛干扰下草原毛虫对小嵩草高寒草甸植物群落特征的影响. 草业科学, 34, 698-705.]
[25]	Mi XC, Feng G, Hu YB, Zhang J, Chen L, Corlett RT, Hughes AC, Pimm S, Schmid B, Shi SH, Svenning JC, Ma KP (2021) The global significance of biodiversity science in China: An overview. National Science Review, 8, nwab032.
[26]	Miehe G, Schleuss PM, Seeber E, Babel W, Biermann T, Braendle M, Chen F, Coners H, Foken T, Gerken T, Graf HF, Guggenberger G, Hafner S, Holzapfel M, Ingrisch J, Kuzyakov Y, Lai Z, Lehnert L, Leuschner C, Li X, Liu J, Liu S, Ma Y, Miehe S, Mosbrugger V, Noltie HJ, Schmidt J, Spielvogel S, Unteregelsbacher S, Wang Y, Willinghöfer S, Xu X, Yang Y, Zhang S, Opgenoorth L, Wesche K (2019) The Kobresia pygmaea ecosystem of the Tibetan highlands—Origin, functioning and degradation of the world’s largest pastoral alpine ecosystem. Science of the Total Environment, 648, 754-771.
[27]	Niu KC, Choler P, Zhao BB, Du GZ (2009) The allometry of reproductive biomass in response to land use in Tibetan alpine grasslands. Functional Ecology, 23, 274-283.
[28]	Niu KC, Chu CJ, Wang ZH (2022) Dynamic niche: A new foundation for rebuilding theory of community ecology. Scientia Sinica (Vitae), 52, 403-417. (in Chinese with English abstract)
	[牛克昌, 储诚进, 王志恒 (2022) 动态生态位: 构建群落生态学理论的新框架. 中国科学: 生命科学, 52, 403-417.]
[29]	Niu KC, He JS, Lechowicz MJ (2016a) Grazing-induced shifts in community functional composition and soil nutrient availability in Tibetan alpine meadows. Journal of Applied Ecology, 53, 1554-1564.
[30]	Niu KC, He JS, Zhang ST, Lechowicz MJ (2016b) Tradeoffs between forage quality and soil fertility: Lessons from Himalayan rangelands. Agriculture, Ecosystems & Environment, 234, 31-39.
[31]	Niu KC, Liu YN, Shen ZH, He FL, Fang JY (2009) Community assembly: The relative importance of neutral theory and niche theory. Biodiversity Science, 17, 579-593. (in Chinese with English abstract) DOI
	[牛克昌, 刘怿宁, 沈泽昊, 何芳良, 方精云 (2009) 群落构建的中性理论和生态位理论. 生物多样性, 17, 579-593.] DOI
[32]	Niu KC, Zhang ST, Lechowicz MJ (2020) Harsh environmental regimes increase the functional significance of intraspecific variation in plant communities. Functional Ecology, 34, 1666-1677.
[33]	Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insect Ecology:Behavior, Populations and Communities. Cambridge University Press, Cambridge.
[34]	Scherber C, Mwangi PN, Temperton VM, Roscher C, Schumacher J, Schmid B, Weisser WW (2006) Effects of plant diversity on invertebrate herbivory in experimental grassland. Oecologia, 147, 489-500. PMID
[35]	Tilman D, Reich PB, Isbell F (2012) Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory. Proceedings of the National Academy of Sciences, USA. 109, 10394-10397.
[36]	Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science, 294, 843-845. PMID
[37]	van der Plas F (2019) Biodiversity and ecosystem functioning in naturally assembled communities. Biological Reviews, 94, 1220-1245.
[38]	Wan XL, Zhang WG (2006) Feeding habit and spatial pattern of Gynaephora alpherakii larvae. Acta Agrestia Sinica, 14, 84-88. (in Chinese with English abstract)
	[万秀莲, 张卫国 (2006) 草原毛虫幼虫的食性及其空间格局. 草地学报, 14, 84-88.] DOI
[39]	Wang L, Delgado-Baquerizo M, Wang DL, Isbell F, Liu J, Feng C, Liu JS, Zhong ZW, Zhu H, Yuan X, Chang Q, Liu C (2019) Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proceedings of the National Academy of Sciences, USA. 116, 6187-6192.
[40]	Wang ZH, Zheng H, Chu CJ, Chen DM, Liu XJ, Wang SP, Niu KC, Tang ZY, Zhou J, Li YQ, Zhang BW, Feng YH (2021) Biodiversity and ecosystem function and service. In: Ecosytem Ecology: Reviews and Prespective (eds Fang JY, Liu LL), pp. 161-212. Higher Education Press, Beijing. FangJY, Liu LL), pp. 161-212. Higher Education Press, Beijing. (in Chinese)
	[王志恒, 郑华, 储诚进, 陈迪马, 刘晓娟, 王少鹏, 牛克昌, 唐志尧, 周健, 李耀琪, 张兵伟, 冯禹昊 (2021) 生物多样性与生态系统功能及服务. 生态系统生态学: 回顾与展望(方精云, 刘玲莉主编), 第161-212页.高等教育出版社, 北京.]
[41]	Wardle DA (2016) Do experiments exploring plant diversity-ecosystem functioning relationships inform how biodiversity loss impacts natural ecosystems? Journal of Vegetation Science, 27, 646-653.
[42]	Wardle DA, Bonner KI, Barker GM, Yeates GW, Nicholson KS, Bardgett RD, Watson RN, Ghani A (1999) Plant removals in perennial grassland: Vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecological Monographs, 69, 535-568.
[43]	Xi XQ, Griffin JN, Sun SC (2013) Grasshoppers amensalistically suppress caterpillar performance and enhance plant biomass in an alpine meadow. Oikos, 122, 1049-1057.
[44]	Yan L, Liu ZK, Mei GR, Lan JH (1995) Feed selection and utilization of grassland caterpillar in the field cage condition. Acta Agrestia Sinica, 3, 257-268. (in Chinese with English abstract)
	[严林, 刘振魁, 梅洁人, 兰景华 (1995) 野外扣笼条件下草原毛虫对食物的选择. 草地学报, 3, 257-268.] DOI
[45]	Yang AL (2002) Serious damage of grassland caterpillars in parts of the Qinghai-Tibet Plateau. Pratacultural Science, 19(5), 73. (in Chinese)
	[杨爱莲 (2002) 西藏青海部分地区草原毛虫为害严重. 草业科学, 19(5), 73.]
[46]	Yu XC, Chen KL, Yao BQ, Ma Z, Wang WY, Wang HC, Zhao XQ, Zhou HK (2016) Effects of simulated warming on the growth and development of Gynaephora menyuanensis larvae. Acta Ecologica Sinica, 36, 8002-8007. (in Chinese with English abstract)
	[余欣超, 陈珂璐, 姚步青, 马真, 王文颖, 王慧春, 赵新全, 周华坤 (2016) 模拟增温下门源草原毛虫幼虫生长发育特征. 生态学报, 36, 8002-8007.]
[47]	Zhang QL, Yuan ML (2013) Research status and prospect of grassland caterpillars (Lepidoptera: Lymantriidae). Pratacultural Science, 30, 638-646. (in Chinese with English abstract)
	[张棋麟, 袁明龙 (2013) 草原毛虫研究现状与展望. 草业科学, 30, 638-646.]
[48]	Zhang ZH, Zhou HK, Zhao XQ, Yao BQ, Ma Z, Dong QM, Zhang ZH, Wang WY, Yang YW (2018) Relationship between biodiversity and ecosystem functioning in alpine meadows of the Qinghai-Tibet Plateau. Biodiversity Science, 26, 111-129. (in Chinese with English abstract) DOI
	[张中华, 周华坤, 赵新全, 姚步青, 马真, 董全民, 张振华, 王文颖, 杨元武 (2018) 青藏高原高寒草地生物多样性与生态系统功能的关系. 生物多样性, 26, 111-129.] DOI
[49]	Zhang ZL, Niu KC, Liu XD, Jia P, Du GZ (2014) Linking flowering and reproductive allocation in response to nitrogen addition in an alpine meadow. Journal of Plant Ecology, 7, 231-239.
[50]	Zheng LL, Song MH, Yin TF, Yu FH (2016) Feeding preference of Gynaephora menyuanensis and its relationships with plant carbon and nitrogen contents in an alpine meadow on the Tibetan Plateau. Acta Ecologica Sinica, 36, 2319-2326. (in Chinese with English abstract)
	[郑莉莉, 宋明华, 尹谭凤, 于飞海 (2016) 青藏高原高寒草甸门源草原毛虫取食偏好及其与植物C、N含量的关系. 生态学报, 36, 2319-2326.]
[51]	Zhong ZW, Li XF, Wang DL (2021) Research progresses of plant-herbivore interactions. Chinese Journal of Plant Ecology, 45, 1036-1048. (in Chinese with English abstract)
	[钟志伟, 李晓菲, 王德利 (2021) 植物-植食性动物相互关系研究进展. 植物生态学报, 45, 1036-1048.] DOI
[52]	Zhou HK, Wang XH, Wen J, Zhu JF, Ye X, Wang WY, Chen Z (2012) The relationship between damage of grassland caterpillar and climate factors in the Maqin County of Guoluo Prefecture. Pratacultural Science, 29, 128-134. (in Chinese with English abstract)
	[周华坤, 王晓辉, 温军, 朱锦福, 叶鑫, 王文颖, 陈哲 (2012) 果洛州玛沁县草原毛虫虫害发生与气候因子的相互关系. 草业科学, 29, 128-134.]
[53]	Zhou XH, Wu WJ, Niu KC, Du GZ (2019) Realistic loss of plant species diversity decreases soil quality in a Tibetan alpine meadow. Agriculture, Ecosystems & Environment, 279, 25-32.