Skip to main content
SpringerLink
Log in

Effects of grazing on C:N:P stoichiometry attenuate from soils to plants and insect herbivores in a semi-arid grassland

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Understanding the processing of limiting nutrients among organisms is an important goal of community ecology. Less known is how human disturbances may alter the stoichiometric patterns among organisms from different trophic levels within communities. Here, we investigated how livestock grazing affects the C:N:P ecological stoichiometry of soils, plants (Leymus chinensis), and grasshoppers (Euchorthippus spp.) in a semi-arid grassland in northeastern China. We found that grazing significantly enhanced soil available N and leaf N content of the dominant L. chinensis grass by 15% and 20%, respectively. Grazing also reduced (soluble) C:N of L. chinensis leaves by 22%. However, grazing did not affect total C, N, or P contents nor their ratios in Euchorthippus grasshoppers. Our results reveal that the effects of grazing disturbances on elemental composition attenuated from lower to higher trophic levels. These findings support the theory that organisms from higher trophic levels have relatively stronger stoichiometric homeostasis compared to those from lower trophic levels. Moreover, grasshopper abundance dropped by 66% in the grazed areas, and they reduced the feeding time on their host L. chinensis grass by 43%, presumably to limit the intake of excess nitrogen from host plants. The energetic costs associated with the maintenance of elemental homeostasis likely reduced grasshopper individual performance and population abundance in the grazed areas. A comprehensive investigation of stoichiometric properties of organisms across trophic levels may enable a better understanding of the nature of species interactions, and facilitate predictions of the consequences of future environmental changes for a community organization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.7d7wm37rq

References

  • Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manag 23:1165–1183

    Article  Google Scholar 

  • Bai Y (2012) Grazing alters ecosystem functioning and C:N: P stoichiometry of grasslands along a regional precipitation gradient. J Appl Ecol 49:1204–1215

    Article  CAS  Google Scholar 

  • Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187

    Article  CAS  PubMed  Google Scholar 

  • Behmer ST, Joern A (2008) Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc Natl Acad Sci USA 105:1977–1982

    Article  CAS  PubMed  Google Scholar 

  • Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci USA 97:14412–14417

    Article  CAS  PubMed  Google Scholar 

  • Belovsky GE, Slade JB, Stockhoff BA (1990) Susceptibility to predation for different grasshoppers—an experimental study. Ecology 71:624–634

    Article  Google Scholar 

  • Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330

    Article  PubMed  Google Scholar 

  • Boersma M, Mathew KA, Niehoff B, Schoo KL, Franco-Santos RM, Meunier CL (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it’s hot? Ecol Lett 19:45–53

    Article  PubMed  Google Scholar 

  • Branco P, Egas M, Elser JJ, Huisman J (2018) Eco-evolutionary dynamics of ecological stoichiometry in plankton communities. Am Nat 192:1–20

    Article  Google Scholar 

  • Cease AJ et al (2012) Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content. Science 335:467–469

    Article  CAS  PubMed  Google Scholar 

  • Cease AJ, Elser JJ, Fenichel EP, Hadrich JC, Harrison JF, Robinson BE (2015) Living with locusts: connecting soil nitrogen, locust outbreaks, livelihoods, and livestock markets. Bioscience 65:551–558

    Article  Google Scholar 

  • Chaneton E et al (1996) Nitrogen and phosphorus cycling in grazed and ungrazed plots in a temperate sub humid grassland in Argentina. J Appl Ecol 33:291–302

    Article  Google Scholar 

  • Chen L, Wang R (2009) Anatomical and physiological divergences and compensatory effects in two Leymus chinensis (Poaceae) ecotypes in Northeast China. Agric Ecosyst Environ 134:46–52

    Article  Google Scholar 

  • Cleveland CC, Liptzin D (2007) C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  • Clissold FJ, Sanson GD, Read J (2006) The paradoxical effects of nutrient ratios and supply rates on an outbreaking insect herbivore, the Australian plague locust. J Anim Ecol 75:1000–1013

    Article  CAS  PubMed  Google Scholar 

  • Daufresne T, Loreau M (2001) Plant-herbivore interactions and ecological stoichiometry: When do herbivores determine plant nutrient limitation? Ecol Lett 4:196–206

    Article  Google Scholar 

  • Delgado-Baquerizo M, Eldridge DJ, Maestre FT, Ochoa V, Gozalo B, Reich PB, Singh BK (2018) Aridity decouples C: N: P stoichiometry across multiple trophic levels in terrestrial ecosystems. Ecosystems 21:459–468

    Article  Google Scholar 

  • Ebell LF (1965) Variation in total soluble sugars of conifer tissues with method of analysis. Phytochemistry 21:227–233

    Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Siemann EH (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    Article  CAS  PubMed  Google Scholar 

  • Elser JJ et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  PubMed  Google Scholar 

  • Elser JJ et al (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608

    Article  CAS  PubMed  Google Scholar 

  • Fagan WF, Denno RF (2004) Stoichiometry of actual vs. potential predator-prey interactions: insights into nitrogen limitation for arthropod predators. Ecol Lett 7:876–883

    Article  Google Scholar 

  • Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802

    Article  PubMed  Google Scholar 

  • Frank DA, Evans RD (1997) Effects of native grazers on grassland N cycling in yellowstone national park. Ecology 78:2238–2248

    Article  Google Scholar 

  • Gusewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Haddad N et al (2001) Contrasting effects of plant richness and composition on insect communities: A field experiment. Am Nat 158:17–35

    Article  CAS  PubMed  Google Scholar 

  • Hawlena D, Schmitz OJ (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci USA 107:15503–15507

    Article  CAS  PubMed  Google Scholar 

  • Hobbs N (1996) Modification of ecosystems by ungulates. J Wildl Manag 60:695–713

    Article  Google Scholar 

  • Hume A et al (2016) Soil C:N: P dynamics during secondary succession following fire in the boreal forest of central Canada. Forest Ecol Manag 369:1–9

    Article  Google Scholar 

  • Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436

    Article  Google Scholar 

  • Joern A, Behmer ST (1997) Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia 112:201–208

    Article  PubMed  Google Scholar 

  • Joern A, Behmer ST (1998) Impact of diet quality on demographic attributes in adult grasshoppers and the nitrogen limitation hypothesis. Ecol Entomol 23:174–184

    Article  Google Scholar 

  • Li X et al (2015) Combined effects of nitrogen addition and litter manipulation on nutrient resorption of Leymus chinensis in a semi-arid grassland of northern China. Plant Biol 17:9–15

    Article  PubMed  Google Scholar 

  • Li X et al (2018) Reciprocal facilitation between large herbivores and ants in a semi-arid grassland. Proc R Soc B Biol Sci 285:20181665

    Article  Google Scholar 

  • Liu C et al (2015a) Effects of grazing on soil nitrogen spatial heterogeneity depend on herbivore assemblage and pre-grazing plant diversity. J Appl Ecol 53:242–250

    Article  Google Scholar 

  • Liu J, Feng C, WangD WL, Wilsey BJ, Zhong Z (2015b) Impacts of grazing by different large herbivores in grassland depend on plant species diversity. J Appl Ecol 52:1053–1062

    Article  Google Scholar 

  • Liu N, Kan HM, Yang GW, Zhang YJ (2015c) Changes in plant, soil, and microbes in a typical steppe from simulated grazing: explaining potential change in soil C. Ecol Monogr 85:269–286

    Article  Google Scholar 

  • McNaughton SJ, Ruess RW, Seagle SW (1988) Large mammals and process dynamics in African ecosystems. Bioscience 38:794–800

    Article  Google Scholar 

  • McSherry ME, Ritchie ME (2013) Effects of grazing on grassland soil carbon: a global review. Glob Chang Biol 19:1347–1357

    Article  PubMed  Google Scholar 

  • Metcalfe DB, Cherif M, Jepsen JU, Vindstad OPL, Kristensen JÅ, Belsing U (2019) Ecological stoichiometry and nutrient partitioning in two insect herbivores responsible for large-scale forest disturbance in the Fennoscandian subarctic. Ecol Entomol 44:118–128

    Article  Google Scholar 

  • Mipam TD, Chen S, Liu J, Miehe G, Tian L (2019) Short-term yak-grazing alters plant-soil stoichiometric relations in an alpine meadow on the eastern Tibetan Plateau. Plant Soil 23:1–13

    Google Scholar 

  • Mulder C, Elser JJ (2009) Soil acidity, ecological stoichiometry and allometric scaling in grassland food webs. Glob Change Biol 15:2730–2738

    Article  Google Scholar 

  • Odum EP (1959) Fundamentals of ecology, 2nd edn. Saunders, Philadelphia

    Google Scholar 

  • Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265

    Article  CAS  PubMed  Google Scholar 

  • Patra AK et al (2005) Effects of grazing on microbial functional groups involved in soil N dynamics. Ecol Monogr 75:65–80

    Article  Google Scholar 

  • Pereira HM et al (2010) Scenarios for global biodiversity in the 21st century. Science 330:1496–1501

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ren BZ (2004) The biology of locusts in Songnen grassland. Science Press, Jilin (in chineses)

    Google Scholar 

  • Riggi LG, Bommarco R (2019) Subsidy type and quality determine direction and strength of trophic cascades in arthropod food webs in agroecosystems. J Appl Ecol 56:1982–1991

    Google Scholar 

  • Risch AC et al (2015) Aboveground vertebrate and invertebrate herbivore impact on net N mineralization in subalpine grasslands. Ecology 96:3312–3322

    Article  PubMed  Google Scholar 

  • Sato C et al (2019) Environmental and grazing management drivers of soil condition. Agric Ecosyst Environ 276:1–7

    Article  CAS  Google Scholar 

  • Schade JD et al (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101

    Article  Google Scholar 

  • Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954

    Article  CAS  PubMed  Google Scholar 

  • Schrama M, Heijning P, Bakker JP, van Wijnen HJ, Berg MP, Olff H (2013) Herbivore trampling as an alternative pathway for explaining differences in nitrogen mineralization in moist grasslands. Oecologia 172:231–243

    Article  PubMed  Google Scholar 

  • Shan Y et al (2011) Seasonally dependent impacts of grazing on soil nitrogen mineralization and linkages to ecosystem functioning in Inner Mongolia grassland. Soil Biol Biochem 43:1943–1954

    Article  CAS  Google Scholar 

  • Simpson SJ, Raubenheimer D (2001) The geometric analysis of nutrient–allelochemical interactions: a case study using locusts. Ecology 82:422–439

    Google Scholar 

  • Sitters J, Bakker ES, Veldhuis MP, Veen GF, Olde Venterink H, Vanni MJ (2017) The stoichiometry of nutrient release by terrestrial herbivores and its ecosystem consequences. Front Earth Sci 5:1–8

    Article  Google Scholar 

  • Sparks DL, Page AL, Loeppert PA, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (1996) Methods of soil analysis part 3: chemical methods. Soil Science Society of America and American Society of Agronomy, Madison

    Book  Google Scholar 

  • Sperfeld E, Wagner ND, Halvorson HM, Malishev M, Raubenheimer D (2017) Bridging ecological stoichiometry and nutritional geometry with homeostasis concepts and integrative models of organism nutrition. Funct Ecol 31:286–296

    Article  Google Scholar 

  • Sterner R, Elser J (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton ((in press))

    Google Scholar 

  • Stout WL et al (1997) Nitrate leaching from cattle urine and feces in Northeast USA. Soil Sci Soc Am J 61:1787–1794

    Article  CAS  Google Scholar 

  • Tian H, Chen G, Zhang C, Melillo JM, Hall CA (2010) Pattern and variation of C: N: P ratios in China’s soils: a synthesis of observational data. Biogeochemistry 98:139–151

    Article  CAS  Google Scholar 

  • van Klink R et al (2015) Effects of large herbivores on grassland arthropod diversity. Biol Rev 90:347–366

    Article  PubMed  Google Scholar 

  • Vanni MJ, McIntyre PB (2016) Predicting nutrient excretion of aquatic animals with metabolic ecology and ecological stoichiometry: a global synthesis. Ecology 97:3460–3471

    Article  PubMed  Google Scholar 

  • Wang J et al (2018) Feces nitrogen release induced by different large herbivores in a dry grassland. Ecol Appl 28:201–211

    Article  PubMed  Google Scholar 

  • Wang L et al (2019) Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proc Natl Acad Sci USA 116:6187–6192

    Article  CAS  PubMed  Google Scholar 

  • Young HS et al (2013) Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. J Ecol 101:1030–1041

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu Q et al (2010) Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol Lett 13:1390–1399

    Article  PubMed  Google Scholar 

  • Zhang Z et al (2014) Grasshoppers regulate N: P stoichiometric homeostasis by changing phosphorus contents in their frass. PLoS ONE 9:e103697

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhong Z, Wang D, Zhu H, Wang L, Feng C, Wang Z (2014) Positive interactions between large herbivores and grasshoppers, and their consequences for grassland plant diversity. Ecology 95:1055–1064

    Article  PubMed  Google Scholar 

  • Zhong Z, Li X, Pearson D, Wang D, Sanders D, Zhu Y, Wang L (2017) Ecosystem engineering strengthens bottom-up and weakens top-down effects via trait-mediated indirect interactions. Proc R Soc B Biol Sci 284:20170475

    Google Scholar 

  • Zhou G et al (2017) Grazing intensity significantly affects belowground carbon and nitrogen cycling in grassland ecosystems: a meta-analysis. Glob Change Biol 23:1167–1179

    Article  Google Scholar 

  • Zhu Y et al (2019) Negative effects of vertebrate on invertebrate herbivores mediated by enhanced plant nitrogen content. J Ecol 107:901–912

    Google Scholar 

Download references

Acknowledgements

Two anonymous reviewers are appreciated for their insightful comments on our manuscript. This project was supported by the National Natural Science Foundation of China (No. 32061143027, 32001384, 31770520), the Program for Introducing Talents to Universities (B16011), the Fundamental Research Funds for the Central Universities (2412020FZ019), and the State Key Laboratory of Grassland Agro-ecosystem of Lan Zhou University (SKLGAE201904).

Author information

Authors and Affiliations

  1. Key Laboratory of Vegetation Ecology/Key Laboratory for Wetland Ecology and Vegetation Restoration, Institute of Grassland Science/School of Environment, Northeast Normal University, Changchun, 130024, Jilin, China

    Nazim Hassan, Jianyong Wang, Hui Zhu, Deli Wang & Zhiwei Zhong

  2. College of Resources and Environmental Sciences/Key Laboratory of Sustainable Utilization of Soil Resources in the Commodity Grain Bases in Jilin Province, Jilin Agricultural University, Changchun, 130118, Jilin, China

    Xiaofei Li

  3. Wetland Ecology Group, Department of Forest Sciences, University of Helsinki, PO Box 27, 00014, Helsinki, Finland

    Petri Nummi

  4. Division of Plant Sciences, University of Missouri, Columbia, USA

    Deborah Finke

Authors
  1. Nazim Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaofei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianyong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hui Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Petri Nummi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Deli Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Deborah Finke
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhiwei Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NH and XFL contributed equally to this work. ZWZ, XFL, and DLW designed experiments; NH, JYW, and HZ performed the experiments and analyzed the data; ZWZ, XFL, DF, PN, DLW, and NH drafted the manuscript; all the authors contributed to the interpretation of results and the critical revision of the manuscript.

Corresponding authors

Correspondence to Deli Wang or Zhiwei Zhong.

Ethics declarations

All experimental procedures were carried out in accordance with the Law of the People’s Republic of China on the Protection of Wildlife (1988).

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Communicated by Diethart Matthies.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hassan, N., Li, X., Wang, J. et al. Effects of grazing on C:N:P stoichiometry attenuate from soils to plants and insect herbivores in a semi-arid grassland. Oecologia 195, 785–795 (2021). https://doi.org/10.1007/s00442-021-04873-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-021-04873-3

Keywords

Search

Navigation