Abstract
Graminoids are typically the dominant plants in certain grassland communities, and their clonal growth is considered an important method of evaluating their adaptation to environmental disturbances. Whether disturbances caused by small burrowing herbivores influence clonal growth in graminoids is not well documented. A field experiment was conducted to investigate the effects of disturbances by small burrowing herbivores, the plateau pika, on the clonal growth of the tussock-forming Kobresia pygmaea and the rhizomatous K. humilis across three sites. This study showed that disturbance by plateau pikas increased the shoot number, spacer number and tiller bud number per clonal fragment of both the tussock-forming K. pygmaea and the rhizomatous K. humilis across three sites. This study also showed that disturbance by plateau pikas increased the rhizome branch number, rhizome length, and rhizome bud number per clonal fragment of rhizomatous K. humilis at each site, while the effects of disturbance by plateau pikas on the rhizome branch number, rhizome length, and rhizome bud number per clonal fragment of the tussock-forming K. pygmaea were different among the three sites. These results suggested that disturbance by plateau pikas benefits for current and potential population recruitment in the tussock-forming K. pygmaea and the rhizomatous K. humilis due to the resulting higher shoot number and tiller bud number per clonal fragment.
Similar content being viewed by others
References
Bakker ES, Ritchie ME, Olff H, Milchunas DG, Knops JMH (2006) Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecol Lett 9:780–788
Benot ML, Mony C, Merlin A, Marion B, Bouzille JB, Bonis A (2011a) Clonal growth strategies along flooding and grazing gradients in Atlantic Coastal Meadows. Folia Geobot 46:219–235. https://doi.org/10.1007/s12224-010-9082-5
Benot ML, Bonis A, Rossignol N, Mony C (2011b) Spatial patterns in defoliation and the expression of clonal traits in grazed meadows. Botany 89:43–54. https://doi.org/10.1139/B10-082
Benson EJ, Hartnett DC (2006) The role of seed and vegetative reproduction in plant recruitment and demography in tallgrass prairie. Plant Ecol 187:163–178. https://doi.org/10.1007/s11258-005-0975-y
Davidson AD, Detling JK, Brown JH (2012) Ecological roles and conservation challenges of social, burrowing, herbivorous mammals in the world's grasslands. Front Ecol Environ 10:477–486. https://doi.org/10.1890/110054
Dobson FS, Smith AT, Gao WX (1998) Social and ecological influences on dispersal and philopatry in the plateau pika (Ochotona curzoniae). Behav Ecol 9:622–635. https://doi.org/10.1093/beheco/9.6.622
Doust LL (1981) Population dynamics and local specialization in a clonal perennial (Ranunculus Repens): II. The dynamics of leaves and a reciprocal transplant-replant experiment. J Ecol 69:743–755. https://doi.org/10.2307/2259634
Fan N, Zhou W, Wei W, Wang Q, Jiang Y (1999) Rodent pest management in the Qinghai-Tibet alpine meadow ecosystem. In: Singleton GR, Hinds LA, Leirs H, Zhang Z (eds) Ecologically-based rodent management. Australian Centre for International Agricultural Research, Canberra, Australia, pp 285–304
Fang HJ, Cheng SL, Yu GR et al (2014) Nitrogen deposition impacts on the amount and stability of soil organic matter in an alpine meadow ecosystem depend on the form and rate of applied nitrogen. Eur J Soil Sci 65:510–519. https://doi.org/10.1111/ejss.12154
Fidelis A, Appezzato-da-Glória B, Pillar VD, Pfadenhauer J (2014) Does disturbance affect bud bank size and belowground structures diversity in Brazilian subtropical grasslands? Flora 209:110–116. https://doi.org/10.1016/j.flora.2013.12.003
Ganie AH, Reshi ZA, Wafai BA, Puijalon S (2016) Clonal growth architecture and spatial dynamics of 10 species of the genus Potamogeton across different habitats in Kashmir Valley, India. Hydrobiologia 767:289–299. https://doi.org/10.1007/s10750-015-2509-5
Gao Y, Xing F, Jin YJ, Nie DD, Wang Y (2012) Foraging responses of clonal plants to multi-patch environmental heterogeneity: spatial preference and temporal reversibility. Plant Soil 359:137–147. https://doi.org/10.1007/s11104-012-1148-0
Gibson DJ (2009) Grasses and grassland ecology. Oxford.
Gough L, Goldberg DE, Hershock C, Pauliukonis N, Petru M (2001) Investigating the community consequences of competition among clonal plants. Evol Ecol 15(54):7–563. https://doi.org/10.1023/A:1016061604630
Gough L, Gross KL, Cleland EE et al (2012) Incorporating clonal growth form clarifies the role of plant height in response to nitrogen addition. Oecologia 169:1053–1062. https://doi.org/10.1007/s00442-012-2264-5
Hendrickson JR, Briske DD (1997) Axillary bud banks of two semiarid perennial grasses occurrence, longevity, and contribution to population persistence. Oecologia 110:584–591. https://doi.org/10.1007/s004420050199
Herben T, Sera B, Klimešová J (2015) Clonal growth and sexual reproduction: tradeoffs and environmental constraints. Oikos 124:469–476. https://doi.org/10.1111/oik.01692
Humphrey LD, Pyke DA (1998) Demographic and growth responses of a guerrilla and a phalanx perennial grass in competitive mixtures. J Ecol 86:854–865. https://doi.org/10.1046/j.1365-2745.1998.8650854.x
Jia S, Wang X, Yuan Z et al (2018) Global signal of top-down control of terrestrial plant communities by herbivores. PNAS 115:6237–6242. https://doi.org/10.1073/pnas.1707984115
Jiang Z (1985) Utilization of the food resource by pateau pika. Acta Theriol Sin 5:251–262. https://doi.org/10.16829/j.slxb.1985.04.003
Jinhua L, Zhenqing L, Jizhou R (2010) Effect of grazing intensity on clonal morphological plasticity and biomass allocation patterns of Artemisia frigida and Potentilla acaulis in the Inner Mongolia steppe. N Zeal J Agric Res 48:57–61. https://doi.org/10.1080/00288233.2005.9513631
Johansen L, Wehn S, Hovstad KA (2016) Clonal growth buffers the effect of grazing management on the population growth rate of a perennial grassland herb. Flora 223:1–18. https://doi.org/10.1016/j.flora.2016.04.007
Jonsdottir IS (1991) Effects of grazing on tiller size and population-dynamics in a clonal sedge (Carex-Bigelowii). Oikos 62:177–188. https://doi.org/10.2307/3545263
Klimešová J, Doležal J, Dvorský M, De Bello F, Klimeš L (2011) Clonal growth forms in eastern Ladakh, Western Himalayas: classification and habitat preferences. Folia Geobot 46:191–217. https://doi.org/10.1007/s12224-010-9076-3
Klimešová J, Tackenberg O, Herben T (2016) Herbs are different: clonal and bud bank traits can matter more than leaf-height-seed traits. New Phytol 210:13–17. https://doi.org/10.1111/nph.13788
Liu Y, Fan J, Shi Z, Yang X, Harris W (2017) Relationships between plateau pika (Ochotona curzoniae) densities and biomass and biodiversity indices of alpine meadow steppe on the Qinghai-Tibet Plateau China. Ecol Eng 102:509–518. https://doi.org/10.1016/j.ecoleng.2017.02.026
Mcnaughton SJ (1983) Compensatory plant-growth as a response to herbivory. Oikos 40:329–336. https://doi.org/10.2307/3544305
Miehe G, Schleuss PM, Seeber E et al (2019) The Kobresia pygmaea ecosystem of the Tibetan highlands-Origin, functioning and degradation of the world's largest pastoral alpine ecosystem: Kobresia pastures of Tibet. Sci Total Environ 648:754–771. https://doi.org/10.1016/j.scitotenv.2018.08.164
Ott JP, Hartnett DC (2014) Bud bank dynamics and clonal growth strategy in the rhizomatous grass, Pascopyrum smithii. Plant Ecol 216:395–405. https://doi.org/10.1007/s11258-014-0444-6
Pang XP, Guo ZG (2017) Plateau pika disturbances alter plant productivity and soil nutrients in alpine meadows of the Qinghai-Tibetan Plateau, China. Rangeland J 39:133–144. https://doi.org/10.1071/RJ16093
Pang XP, Guo ZG (2018) Response of leaf traits of common plants in alpine meadow to plateau pika disturbance. Rangeland J 40:39–46. https://doi.org/10.1071/Rj17089
Pang XP, Wang Q, Zhang J et al (2019) Responses of soil inorganic and organic carbon stocks of alpine meadows to the disturbance by plateau pikas. Eur J Soil Sci. https://doi.org/10.1111/ejss.12895
Pang XP, Yu CQ, Zhang J, Wang Q, Guo ZG, Tian Y (2020) Effect of disturbance by plateau pika on soil nitrogen stocks in alpine meadows. Geoderma 372:114392. https://doi.org/10.1016/j.geoderma.2020.114392
Pottier J, Evette A (2010) On the relationship between clonal traits and small-scale spatial patterns of three dominant grasses and its consequences on community diversity. Folia Geobot 45:59–75. https://doi.org/10.1007/s12224-009-9053-x
Qian J, Wang Z, Liu Z, Busso CA (2014) Belowground bud bank responses to grazing intensity in the Inner-Mongolia Steppe, China. Land Degrad Dev 28:822–832. https://doi.org/10.1002/ldr.2300
Rusch GM, Wilmann B, Klimešová J, Evju M (2010) Do clonal and bud bank traits vary in correspondence with soil properties and resource acquisition strategies? Patterns in Alpine communities in the Scandian mountains. Folia Geobot 46:237–254. https://doi.org/10.1007/s12224-010-9072-7
Smith AT, Badingqiuying WMC, Hogan BW (2019) Functional-trait ecology of the plateau pika Ochotona curzoniae in the Qinghai-Tibetan Plateau ecosystem. Integr Zool 14:87–103. https://doi.org/10.1111/1749-4877.12300
Sun F, Chen W, Liu L, Liu W, Cai Y, Smith P (2015) Effects of plateau pika activities on seasonal plant biomass and soil properties in the alpine meadow ecosystems of the Tibetan Plateau. Grassl sci 61:195–203. https://doi.org/10.1111/grs.12101
VanderWeide BL, Hartnett DC (2015) Belowground bud bank response to grazing under severe, short-term drought. Oecologia 178:795–806. https://doi.org/10.1007/s00442-015-3249-y
Van Staalduinen MA, Werger MJA (2007) Marmot disturbances in a Mongolian steppe vegetation. J Arid Environ 69:344–351. https://doi.org/10.1016/j.jaridenv.2006.08.002
Wang Z, Li L, Han X, Dong M (2004) Do rhizome severing and shoot defoliation affect clonal growth of Leymus chinensis at ramet population level? Acta Oecol 26:255–260. https://doi.org/10.1016/j.actao.2004.08.007
Wang W, Ma Y, Xu J, Wang H, Zhu J, Zhou H (2012) The uptake diversity of soil nitrogen nutrients by main plant species in Kobresia humilis alpine meadow on the Qinghai-Tibet Plateau. Sci China Earth Sci 55:1688–1695. https://doi.org/10.1007/s11430-012-4461-9
Wang Q, Yu C, Pang XP, Jin SH, Zhang J, Guo ZG (2018) The disturbance and disturbance intensity of small and semi-fossorial herbivores alter the belowground bud density of graminoids in alpine meadows. Ecol Eng 113:35–42. https://doi.org/10.1016/j.ecoleng.2018.01.003
Ye XH, Yu FH, Dong M (2006) A trade-off between guerrilla and phalanx growth forms in Leymus secalinus under different nutrient supplies. Ann Bot 98:187–191. https://doi.org/10.1093/aob/mcl086
Ye XH, Gao SQ, Liu ZL, Zhang YL, Huang ZY, Dong M (2015) Multiple adaptations to light and nutrient heterogeneity in the clonal plant Leymus secalinus with a combined growth form. Flora 213:49–56. https://doi.org/10.1016/j.flora.2015.04.006
Yu C, Pang XP, Wang Q, Jin SH, Shu CC, Guo ZG (2017) Soil nutrient changes induced by the presence and intensity of plateaupika (Ochotona curzoniae) disturbances in the Qinghai-Tibet Plateau, China. Ecol Eng 106:1–9. https://doi.org/10.1016/j.ecoleng.2017.05.029
Zhang HY, Wang Q, Yu C, Pang XP, Jin SH, Guo ZG (2018) Effect of plateau pika disturbance on reproductive allocation of Kobresia pygmaea. Pratacult Sci. https://doi.org/10.11829/j.issn.1001-0629.2017-0272
Zhang WN, Wang Q, Zhang J et al (2020) Effect of clipping behavior by plateau pika on plant community. Rangeland Ecol Manag 73:368–374. https://doi.org/10.1016/j.rama.2020.01.010
Zheng Z, Bai W, Zhang WH (2019) Clonality-dependent dynamic change of plant community in temperate grasslands under nitrogen enrichment. Oecologia 189:255–266. https://doi.org/10.1007/s00442-018-4317-x
Acknowledgements
The authors would like to thank Chao Cheng Shu, Shao Hong Jin, Hong Yan Zhang, Hai Peng Xu, Wen Na Zhang, Juan Wang, Ding Yang, Ying Ying Chen, Jie Li, Di Gang Zhi, Fu Yun Qiao, Hao Hao Qi and Gan Lin Feng from Lanzhou University, and Xuan Dun Lin and Wen Li Wu from Northwest Minzu University for their field assistance and laboratory analysis that contributed to this study. This study was funded by the Changjiang Scholars and Innovative Research Team in University (IRT17R50), the Major Special Project for Improvement and Utilization of Forage Germplasm in Tibetan Autonomous Region (XZ201901NA03), and the National Natural Science Foundation of China (31172258).
Funding
This study was funded by the Changjiang Scholars and Innovative Research Team in University (IRT17R50), the Major Special Project for Improvement and Utilization of Forage Germplasm in Tibetan Autonomous Region (XZ201901NA03), and the National Natural Science Foundation of China (31172258).
Author information
Authors and Affiliations
Contributions
QW, and ZGG designed the research, QW, XPP, JZ and HY conducted the research, and QW and ZGG analyzed the data and wrote the article.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The Kobresia pygmaea and K. humilis are not endangered and endemic species.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, Q., Guo, Z.G., Pang, X.P. et al. Effects of small-herbivore disturbance on the clonal growth of two perennial graminoids in alpine meadows. Alp Botany 130, 115–127 (2020). https://doi.org/10.1007/s00035-020-00240-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00035-020-00240-9