Skip to main content

Linking changes of forage production and digestibility with grassland community assembly under nitrogen enrichment



Forage production is the fundamental ecosystem service of grasslands. Although forage consumption occurs at community level, most studies focused on species-level changes of forage quality. The quantitative and qualitative changes of forage production are driven by species-specific trait, intra-specific plasticity, and species turnover. We examined the changes in forage production and digestibility after 5-year factorial treatments of nitrogen (N) addition and mowing in a temperate steppe and linked such changes to community assembly under the Price equation framework.


Nitrogen addition significantly reduced species richness, increased forage production, but did not change forage digestibility (indicated by the total Ca+Mg concentrations). Mowing did not affect forage production and digestibility. The positive effects of N addition on forage production were driven by the enhancement of abundance of the remaining species following N enrichment, rather than by species loss or species gain. The species identity effects could offset the effects of species richness loss or gain on forage production and digestibility.


Our results highlight the importance of a community perspective in addressing the quantitative and qualitative changes of forage production under global change pressure of N enrichment. Species identity is important in determining the contribution of different processes of community assembly to ecosystem services.


Grasslands, the largest terrestrial biome on earth, provide important goods and services (Gibson 2009). Forage production ranks among a fundamental grassland ecosystem service, with the productivity and quality of forage largely depending upon species diversity and community composition. While positive relationships between plant species diversity and primary production are widely reported (Hooper et al. 2005; Tilman et al. 2014), the relationship between community composition and primary production remains largely unknown (Bannar-Martin et al. 2018). Further, compared with our knowledge about the quantitative changes of primary production in response to the changes of biodiversity and community composition, much less is understood about its qualitative changes, such as the forage digestibility. Such knowledge gaps hinder our ability to predict the responses of grassland fundamental services to global change drivers, because both plant diversity and community composition in grasslands are sensitive to global changes (Zavaleta et al. 2003).

Increased atmospheric nitrogen (N) deposition is one of the most widespread global change drivers, which threatens biodiversity and alters community composition in grasslands (Bobbink et al. 2010). Nitrogen enrichment facilitates the growth of perennial grasses with high stature but inhibits forbs due to light limitation (Hautier et al. 2009), resource competition (Dickson and Foster 2011), and ammonia or metal toxicity (Tian et al. 2016). These factors consequently alter native grassland plant community composition (Dupre et al. 2010; Zhang et al. 2015). Although positive effects of N enrichment on primary productivity in grasslands are widely reported (LeBauer and Treseder 2008), the losses of species richness could substantially diminish such positive effects of N enrichment in the long-term (Isbell et al. 2013). Beyond species richness, species identity is another important determinant of primary productivity, as plant species differ in their responses to N enrichment due to their variation in evolutionary history and functional traits (Wooliver et al. 2017). In a tallgrass prairie, Avolio et al. (2014) found that the shifts of community composition from C4 grasses to forbs (rather than change in species richness) drove temporal variation of primary productivity in response to long-term N addition. Moreover, mowing for forage in grasslands plays an important role in mediating the impacts of N addition on community composition (Yang et al. 2019). Species richness and community composition are closely related with community assembly processes. While the role of community assembly in driving ecosystem functioning including primary productivity is theoretically highlighted (Leibold et al. 2017), empirical evidence is rather scarce.

Forage digestibility is as important as the amount of forage production, because it represents the amount of energy available for livestock (Bruinenberg et al. 2002). Due to substantial inter-specific variation in forage digestibility and intra-specific responses to environmental changes, the community-level forage digestibility is sensitive to factors that can alter plant community composition, including nutrient availability, disturbance regime, and climatic factors (Pontes et al. 2007; Gardarin et al. 2014). Summing plant calcium (Ca) and magnesium (Mg) concentrations is a meaningful indicator of forage digestibility (Mladkova et al. 2018), because both elements are important for the production of soft tissues and easily digestible vegetative material (Hawkesford et al. 2012; Maathuis 2009). Forbs generally have higher Ca and Mg concentrations than grasses (Han et al. 2011), and thus have higher digestibility (Duru 1997; Mladkova et al. 2018). Consequently, reduced forb biomass and the paralleled increases of grass biomass following N enrichment as observed in diverse grasslands may lead to lower forage digestibility. In contrast, mowing would results in higher forage digestibility at community level by facilitating the growth of forbs but decreasing that of grasses. Further, the stimulation of plant growth by N enrichment has carbon:nutrient dilution effects in plant tissue (Tian et al. 2019), including Ca and Mg, which might negatively affect forage digestibility.

Identifying how N enrichment affects the relative contribution of intra-specific (due to physiological alterations) and inter-specific changes (due to species loss and gain) would improve our mechanistic understanding of the responses of community-level forage digestibility. However, to date, there are few attempts to assess the relative importance of intra- and inter-specific changes in driving community-level alteration of the total amount and digestibility of forage production. Empirical evidence shows that the ecological version of Price equation developed by Fox (2006) could successfully partition the contributions of species loss, species gain, and intra-specific physiological changes to ecosystem function and properties (Teurlincx et al. 2017; Bannar-Martin et al. 2018). By comparing the differences in function between a baseline community and a comparison community, the extended Price equation could partition such differences into five components: (1) species richness effect of losses (SRE.L) which represents the extent by which the function has changes as a result of random loss of species with perfectly average function from the baseline community, (2) species identity effect of losses (SIE.L) which represents the effects of losing species with higher or lower function than average functioning species in the baseline community, (3) species richness effect of gains (SRE.G) which reflects the contribution of random gaining species with perfectly average function in the comparison community, (4) species identity effect of gains (SIE.G) which reflects the contribution of gaining species with higher or lower function than the average functioning species in the comparison community, and (5) context-dependent effect of resident species (CDE) which reflects the contribution of intra-specific physiological changes of shared species by baseline community and comparison community (Winfree et al. 2015; Bannar-Martin et al. 2018). Consequently, the Price equation framework could provide a quantitative link between community assembly and ecosystem function.

Here, we examined the impacts of N enrichment on forage production and digestibility with a factorial field experiment with N addition and mowing in a temperate meadow steppe, and further quantitatively linked such changes with different processes of community assembly. We hypothesized that (1) CDE would be the main contributor to the enhancement of forage production following N addition, as evidenced in literature that grasses are always facilitated by N enrichment (Dupre et al. 2010; Zhang et al. 2015), (2) N addition would reduce forage digestibility (indicated by lower total concentrations of Ca and Mg) due to the losses of forbs and the intra-specific variation of resident species, but (3) such impacts of N addition would be less strong under mowing conditions, as mowing can mitigate the effects of N addition on species richness and the growth of dominant grass in this ecosystem (Yang et al. 2019).

Materials and methods

Study site

The experimental site—a natural meadow steppe near the Erguna Forest-Steppe Ecotone Research Station (50° 10′ 46.1′′N, 119° 22′ 56.4′′E, 650 m a.s.l.)—has been fenced since 2013 to prevent livestock grazing. Prior to 2013, the site had been annually mown for hay-harvesting. The mean annual precipitation from 1957 to 2018 is 360 mm and the mean annual temperature is −2.4 °C. The soil is classified as chernozem in the Chinese Soil Taxonomy. The pH of surface soil (0–10 cm) is 6.8–7.0. The concentration of soil organic carbon, total N, and total phosphorus in the surface layer is 25 g C kg−1, 2.4 g N kg−1, and 0.7 g P kg−1, respectively. The dominant plant species are Leymus chinensis, Stipa baicalensis, Cleistogenes squarrosa, Thermopsis lanceolate, Cymbaria dahurica, and Carex duriuscula. Mowing for forage harvest is a common management practice in this area.

Experimental design

The experiment was established in 2014 following a factorial design with two factors: N addition and mowing, resulting in four treatments (control, N addition, mowing, combined N addition and mowing). Five replicates (n = 5) of each treatment were distributed in five blocks, with twenty 10 m × 10 m plots in total. Plots were separated by 1 m walkways. Annual N addition occurred from 2014–2018; powdered NH4NO3 was added at a rate of 10 g N m−2 year−1 in mid-May of each year. We chose such a N addition rate for the convenience of results comparison among different studies. Plots under the mowing treatments were mown with a mower about 10 cm above the soil surface at the end of August each year. All the plant tissue was removed to the edge of each plot after mowing.

In mid-August of 2018, during the annual peak in aboveground biomass, living shoots were sampled by clipping all vascular plants in a 1 m × 1 m quadrat randomly placed in each plot (50 cm inside each plot to avoid edge effect). Plants in each quadrat were sorted to species, oven-dried at 65 °C for 48 h, and then weighed and ground. Plant samples were acid digested with a mixture of acids (HNO3:HClO4 = 5:1) in a microwave oven. The concentrations of Ca and Mg in the solution were measured using inductively coupled plasma mass spectrometry (Perkin Elmer, ELAN-6000).

To clarify the roles of different Price components to the N-induced variation of forage production under unmowed and mown (M) conditions, we calculated the contribution of SRE.L, SIE.L, SRE.G, SIE.G, and CDE to the difference of forage production between control plot (as baseline community) and +N plot (as comparison community) in each block and between mown plot (as baseline community) and +NM plot (as comparison community) in each block, separately. Following the method developed by Fox and Kerr (2012) and Bannar-Martin et al. (2018), the contribution of each of the five components was calculated as:

SRE.L = (ScS)\( \overline{\mathrm{z}} \) (1)

SIE.L = Sc(\( \overline{\mathrm{z}} \)c\( \overline{\mathrm{z}} \)) (2)

SRE.G = (S′−Sc)\( \overline{\mathrm{z}}\hbox{'} \) (3)

SIE.G = −Sc(\( \overline{\mathrm{z}}\hbox{'} \)c\( \overline{\mathrm{z}}\hbox{'} \)) (4)

CDE = Sc(\( \overline{\mathrm{z}}\hbox{'} \)c\( \overline{\mathrm{z}} \)c) (5)

in which, S, S′, and Sc is the number of species in the baseline community, the comparison community, and that shared by baseline community and comparison community, respectively; \( \overline{\mathrm{z}} \), \( \overline{\mathrm{z}}\hbox{'} \), \( {\overline{\mathrm{z}}}_{\mathrm{c}} \), and \( \overline{\mathrm{z}}{\hbox{'}}_{\mathrm{c}} \) is the averaged biomass at species-level for all the species in the baseline community, the comparison community, and that for shared species in the baseline community and the comparison community.

Because the partitions of element concentration could not be directly summed, we evaluated the relative contribution of each Price component (pj) on the N-induced variation of community-level summing of Ca and Mg concentrations (CM) following the method of Teurlincx et al. (2017), which based on the contribution of each component to the changes of nutrient content (NC) and biomass (B) in the comparison community:

ΔCMpj = ((NCbase + ΔNCpj)/(Bbase + ΔBpj)) ‐ (NCbase/Bbase) (9) in which, NCbase refers to the summing content of Ca and Mg in base community, Bbase refers to the biomass of base community, ΔNCpj refers to changes of Ca and Mg content due to the component pj, and ΔBpj refers to changes of biomass due to the component pj. The contribution of SRE.L to the changes of community-level summing of Ca and Mg concentrations is zero, because random loss of species with average nutrient concentration would not affect the community-level nutrient concentration.

Statistical analysis

Normal distribution and homogeneity of variances of all data were checked with Kolmogorov-Smirnov test and Levene’s test, respectively. Results showed all the data met such assumptions. With all the four treatments being combined, the differences of summed Ca and Mg concentration between forbs and grasses were detected using t tests. To detect the main and interactive effects of N addition and mowing on species richness, forage production, and concentration of Ca and Mg, three-way ANOVAs were performed with N addition and mowing as the fixed factors and block as random factor. The t tests were used to test the differences of the contribution of each component from 0. All data analyses were performed with SPSS version 20.0 (SPSS, Chicago, IL, USA).


Nitrogen addition significantly reduced total species richness (Fig. 1a) and forb species richness (Fig. 1b), but did not affect the species richness of grasses (Fig. 1c). The losses of species richness were due to higher species loss than species gain, with both being significantly higher than 0, indicating the occurrence of species turnover following N addition (Fig. S1). In most cases, more forb species than grass species being lost or gained during the species turnover induced by N addition under both mown and unmown conditions (Table S1). Mowing did not affect species richness of the whole community, forbs, and grasses (Fig. 1).

Fig. 1
figure 1

Effects of nitrogen addition and mowing on species richness of the whole community (a), forbs (b), and grasses (c). N0, no N addition; +N, N addition. Data are presented as means ±1 SEM. ANOVA P values are reported when P < 0.05

Nitrogen addition significantly enhanced forage production at community level and for grasses, with no effect on forbs (Fig. 2). Nitrogen addition increased community-level forage production by 120 g m−2 under unmown conditions, and by 180 g m−2 under mown conditions (Fig. 2a). Nitrogen addition did not affect the summed concentrations of Ca+Mg in forage at either the community or functional group level (Fig. 3). Across all the treatments, the biomass-weighted concentration of Ca+Mg in forbs was three times higher than that in grasses (1.47% vs 0.43%; Fig. 3). Mowing had no impact on forage production and the summed concentrations of Ca+Mg at all examined levels (Figs. 1, 2, 3).

Fig. 2
figure 2

Effects of nitrogen addition and mowing on forage production of the whole community (a), forbs (b), and grasses (c). N0, no N addition; +N, N addition. Data are presented as means ±1 SEM. ANOVA P values are reported when P < 0.05

Fig. 3
figure 3

Effects of nitrogen addition and mowing on plant Ca+Mg concentrations averaged across the whole community (a), forbs (b), and grasses (c). N0, no N addition; +N, N addition. Data are presented as means ±1 SEM. ANOVA P values are reported when P < 0.05

Under both unmown and mown conditions, almost all the Price components significantly contributed to the N-induced changes of community-level forage production (Fig. 4a). Random species richness loss contributed negatively and the identity of species loss contributed positively to the changes of forage production (Fig. 4a). Random species gain contributed positively but the identity of gained species contributed negatively to the changes of forage production (Fig. 4a). The growth of species shared between the baseline and comparison communities was stimulated by N addition as indicated by the positive CDE values (Fig. 4a).

Fig. 4
figure 4

Price partitions of changes in forage production (a) and Ca+Mg concentrations (b) between the treatments with and without N addition under unmown and mown conditions. SRE.L, species richness effect of species loss; SIE.L, species identity effect of species loss; SRE.G, species richness effect of species gain; SIE.G, species identity effect of species gain; CDE, context dependent effect. Significance levels of the changes different from 0 were assessed using t tests. ns, P > 0.1; ^, 0.05 < P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001

Nearly all Price components did not significantly contribute to the N-induced changes of Ca+Mg concentration at community level (Fig. 4b). One exception was the identity of species loss when N was added under unmown conditions, which negatively contributed to changes of Ca+Mg concentration (Fig. 4b).


Our results showed that N enrichment significantly enhanced forage production under both mown and unmown conditions, but did not affect forage digestibility as indicated by its neutral impact on the summed Ca+Mg concentrations in forage. Under the framework of the extended Price equation, we quantified the contribution of species loss, species gain, and intra-specific variation to the changes of forage production and digestibility in response to N enrichment. The increases of forage production following N enrichment were contributed by the positive CDE that is the enhancement of intra-specific growth of shared species between communities with and without N addition. Although there were substantial forb species losses following N enrichment and the digestibility of forbs is greater than that of grasses, forage digestibility was not affected by N enrichment due to the offset among different community assembly processes.

Consistent with our first hypothesis, species shared by control and N-enriched communities (CDE component) had a positive contribution to the N-induced increases of forage production. While it is widely known that N fertilization enhances primary productivity in diverse grasslands (Elser et al. 2007; Zhang et al. 2015), our study is among the first to link such changes of production with community assembly processes (Fox and Kerr 2012). Nitrogen enrichment reduces species richness in diverse grasslands and consequently alters ecosystem functioning (Isbell et al. 2013; Zhang et al. 2014). The reduction of species richness following N enrichment reflects species turnover with both species loss and species gain. Unfortunately, few studies have examined the relative contribution of species loss and species gain to changes of ecosystem functioning and services (Bannar-Martin et al. 2018).

There are several novel findings from our study. Species richness losses following N enrichment negatively influenced forage production, as indicated by the negative contribution of SRE.L. Many studies report lower primary productivity associated with species loss (Isbell et al. 2013; Tilman et al. 2014). However, species losses following N enrichment are often non-random due to functional- and abundance-based mechanisms (Suding et al. 2005). In our ecosystem, forb species richness was much more sensitive to N addition than would be expected by chance, with a significant reduction of forb richness following N addition. As their contribution to forage production was lower than that of grasses (Fig. 2b, c), the losses of forbs drove a lower reduction of forage production than expected due to species random losses. Consequently, we found significant positive contribution of SIE.L component to changes of forage production, which offset the negative effects of SRE.L. These findings highlight the importance of species identity in modulating the impacts of species losses on forage production under N enrichment.

Species identity was important in determining the impacts of species gain on the changes of forage production. We observed that both species richness effect of gains (SRE.G) and species identity effect of gains (SIE.G) significantly contributed to the changes in forage production observed following N enrichment, with positive contribution of SRE.G and negative contribution of SIE.G. All species presented in the comparison community (N enriched) has positive contribution to forage production, and consequently a positive effects of SRE.G being found. The negative contribution of SIE.G implies that the production of gained species following N enrichment was generally lower than that averaged across all the species, which consequently offset the positive effects of SRE.G.

In contrast to our hypothesis, N addition did not significantly affect forage digestibility. The SRE.L component, which was quantified by the mean values of nutrient concentrations average across all species in the baseline community (no N addition or mowing), did not contribute to the changes of community level nutrient concentrations (Teurlincx et al. 2017). Forb species had higher Ca+Mg concentrations than grasses, indicating higher forage digestibility, which is consistent with results from previous studies (Duru 1997; Gardarin et al. 2014). We found that N addition significantly decreased species richness of forbs, negatively impacting forage digestibility as indicated by the contribution of SIE.L component (Fig. 4b). Notably, the negative contribution of SIE.L to changes of forage digestibility was statistically significant only under the unmown conditions. In a previous study, we found that mowing could mediate the negative effects of N deposition on plant species diversity by suppressing the competitive advantage of dominant grass species across a N addition gradient ranging from 0–50 g N m−2 year−1 (Yang et al. 2019). In this study, however, we found no interactive effect between N addition and mowing. Such contrasting results indicate that the mediating role of mowing on the negative effects of N addition on species diversity would depend on the rates of N addition and may vary among different years. The negative impacts of SIE.L did not lead to changes of Ca+Mg concentration at community level, because its effect was offset by SIE.G.

There were substantial species gains following N enrichment, though the number of species gained was less than that of species loss. However, both the richness and identity of species gained after N enrichment did not significantly impact forage Ca+Mg concentrations, indicating the species gain process did not affect forage digestibility in this ecosystem. Together with the finding that both SRE.G and SIE.G significantly affected forage production, our results indicate that the species gain process had divergent effects on the quantity and quality of forage production. Similarly, we found that CDE did not contribute to the changes of forage digestibility, indicating that the summed concentrations of Ca+Mg in the plant species shared by communities with and without N addition were not changed by N addition. However, the biomass Ca+Mg storage in forage must be increased by N addition because the significant enhancement of forage production. Such increases of plant Ca+Mg uptake following N addition may reduce soil extractable Ca and Mg concentrations under N enrichment as reported in the temperate steppe (Wang et al. 2018). While cation leaching induced by soil acidification following N enrichment has been widely reported (Lucas et al. 2011; Wang et al. 2018), the potential decreases of soil exchangeable base cation due to plant uptake after N enrichment should receive more attention, especially in the grassland being used for forage harvest.


Nitrogen addition with a rate of 10 g m−2 year−1 significantly increased forage production but did not alter forage digestibility in a meadow steppe. Following the Price equation framework, we linked such responses of forage production and forage digestibility to community assembly processes. While the effects of both species richness loss and gain significantly affected forage production, as predicted by previous studies, our results showed that the identities of species being lost and gained could offset the effects of random species richness loss and gain. Our results highlight the importance of species identity in driving the contribution of community assembly processes to forage production following N enrichment. Because N addition significantly enhanced the quantity of forage production but did not change forage quality, N fertilization should be an important management strategy to enhance ecosystem services in the meadow steppe.

Availability of data and materials

The datasets used during the current study are available from the corresponding author on reasonable request.


  1. Avolio ML, Koerner SE, La Pierre KJ, Wilcox KR, Wilson GWT, Smith MD, Collins SL (2014) Changes in plant community composition, not diversity, during a decade of nitrogen and phosphorus additions drive above-ground productivity in a tallgrass prairie. J Ecol 102(6):1649–1660.

    CAS  Article  Google Scholar 

  2. Bannar-Martin KH, Kremer CT, Morgan Ernest SK, Leibold MA, Auge H, Chase J, Declerck SAJ, Eisenhauer N, Harpole S, Hillebrand H, Isbell F, Koffel T, Larsen S, Narwani A, Petermann JS, Roscher C, Cabral JS, Supp SR (2018) Integrating community assembly and biodiversity to better understand ecosystem function: the community assembly and the functioning of ecosystems approach. Ecol Lett 21(2):167–180.

    Article  Google Scholar 

  3. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20(1):30–59.

    CAS  Article  Google Scholar 

  4. Bruinenberg MH, Valk H, Korevaar H, Struik PC (2002) Factors affecting digestibility of temperate forages from seminatural grasslands: a review. Grass Forage Sci 57(3):292–301.

    Article  Google Scholar 

  5. Dickson TL, Foster BL (2011) Fertilization decreases plant biodiversity even when light is not limiting. Ecol Lett 14(4):380–388.

    Article  Google Scholar 

  6. Dupre C, Stevens CJ, Ranke T, Bleeker A, Peppler-Lisbach C, Gowing DJG, Dise NB, Dorland E, Bobbink R, Diekmann M (2010) Changes in species richness and composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Glob Change Biol 16(1):344–357.

    Article  Google Scholar 

  7. Duru M (1997) Leaf and stem in vitro digestibility for grasses and dicotyledons of meadow plant communities in spring. J Sci Food Agr 74(2):175–185.<175::AID-JSFA787>3.0.CO;2-V

    CAS  Article  Google Scholar 

  8. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10(12):1135–1142.

    Article  Google Scholar 

  9. Fox JW (2006) Using the price equation to partition the effects of biodiversity loss on ecosystem function. Ecology 87(11):2687–2696.[2687:UTPETP]2.0.CO;2

    Article  Google Scholar 

  10. Fox JW, Kerr B (2012) Analyzing the effects of species gain and loss on ecosystem function using the extended Price equation partition. Oikos 121(2):290–298.

    Article  Google Scholar 

  11. Gardarin A, Garnier E, Carrere P, Cruz P, Andueza D, Bonis A, Colace MP, Dumont B, Duru M, Farruggia A, Gaucherand S, Grigulis K, Kemeis E, Lavorel S, Louault F, Loucougaray G, Mesleard F, Yavercovski N, Kazakou E (2014) Plant trait-digestibility relationships across management and climate gradients in permanent grasslands. J Appl Ecol 51(5):1207–1217.

    Article  Google Scholar 

  12. Gibson DJ (2009) Grasses and grassland ecology. Oxford University Press, Oxford

    Google Scholar 

  13. Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14(8):788–796.

    CAS  Article  Google Scholar 

  14. Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324(5927):636–638.

    CAS  Article  Google Scholar 

  15. Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of macronutrients. In: Marschner P (ed) Marschner’s Mineral Nutrition of Higher Plants, 3rd edn. Academic Press, London, pp 135–190

    Chapter  Google Scholar 

  16. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monog 75(1):3–35.

    Article  Google Scholar 

  17. Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S (2013) Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc Nat Acad Sci USA 110(29):11911–11916.

    Article  Google Scholar 

  18. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89(2):371–379.

    Article  Google Scholar 

  19. Leibold MA, Chase JM, Ernest SKM (2017) Community assembly and the functioning of ecosystems: how metacommunity processes alter ecosystem attributes. Ecology 98(4):909–919.

    Article  Google Scholar 

  20. Lucas RW, Klaminder J, Futter MN, Bishopc KH, Egnell G, Laudona H, Högberga P (2011) A meta-analysis of the effects of nitrogen additions on base cations: implications for plants, soils, and streams. Forest Ecol Manage 262(2):95–104.

    Article  Google Scholar 

  21. Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12(3):250–258.

    CAS  Article  Google Scholar 

  22. Mladkova P, Mladek J, Hejduk S, Hejcman M, Pakeman RJ (2018) Calcium plus magnesium indicates digestibility: the significance of the second major axis of plant chemical variation for ecological processes. Ecol Lett 21(6):885–895.

    Article  Google Scholar 

  23. Pontes LS, Carrere P, Andueza D, Louault F, Soussana JF (2007) Seasonal productivity and nutritive value of temperate grasses found in semi-natural pastures in Europe: response to cutting frequency and N supply. Grass Forage Sci 62(4):485–496.

    CAS  Article  Google Scholar 

  24. Suding KN, Collins SL, Gough L, Clark CM, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Nat Acad Sci USA 102(12):4387–4392.

    CAS  Article  Google Scholar 

  25. Teurlincx S, Velthuis M, Seroka D, Govaert L, van Donk E, Van de Waal DB, Declerck SAJ (2017) Species sorting and stoichiometric plasticity control community C:P ratio of first-order aquatic consumers. Ecol Lett 20(6):751–760.

    Article  Google Scholar 

  26. Tian DS, Reich PB, Chen HYH, Xiang YZ, Luo YQ, Shen Y, Meng C, Han WX, Niu SL (2019) Global changes alter plant multi-element stoichiometric coupling. New Phytol 221(2):807–817.

    CAS  Article  Google Scholar 

  27. Tian Q, Liu N, Bai W, Li L, Chen J, Reich PB, Yu Q, Guo D, Smith M, Knapp AK, Cheng W, Lu P, Gao Y, Yang A, Wang T, Li X, Wang Z, Ma Y, Han X, Zhang W (2016) A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97(1):65–74.

    Article  Google Scholar 

  28. Tilman D, Forest I, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45(1):471–493.

  29. Wang RZ, Zhang YH, He P, Yin JF, Yang JJ, Liu HY, Cai JP, Shi Z, Feng X, Dijkstra FA, Han XG, Jiang Y (2018) Intensity and frequency of nitrogen addition alter soil chemical properties depending on mowing management in a temperate steppe. J Environ Manag 224:77–86.

    CAS  Article  Google Scholar 

  30. Winfree R, Fox JW, Williams NM, Reilly JR, Cariveau DP (2015) Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol Lett 18(7):626–635.

    Article  Google Scholar 

  31. Wooliver RC, Marion ZJ, Peterson CR, Potts BM, Senior JK, Bailey JK, Schweitzer JA (2017) Phylogeny is a powerful tool for predicting plant biomass responses to nitrogen enrichment. Ecology 98(8):2120–2132.

    Article  Google Scholar 

  32. Yang GJ, Lü XT, Stevens CJ, Zhang GM, Wang HY, Wang ZW, Zhang ZJ, Liu ZY, Han XG (2019) Mowing mitigates the negative impacts of N addition on plant species diversity. Oecologia 189(3):769–779.

    Article  Google Scholar 

  33. Zavaleta ES, Shaw MR, Chiariello NR, Mooney HA, Field CB (2003) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc Nat Acad Sci USA 100(13):7650–7654.

    CAS  Article  Google Scholar 

  34. Zhang YH, Feng JC, Isbell F, Lü XT, Han XG (2015) Productivity depends more on the rate than the frequency of N addition in a temperate grassland. Sci Rep 5(1):12558.

    CAS  Article  Google Scholar 

  35. Zhang YH, Lü XT, Isbell F, Stevens C, Han X, He NP, Zhang GM, Yu Q, Huang JH, Han XG (2014) Rapid plant species loss at high rates and at low frequency of N addition in temperate steppe. Glob Change Biol 20(11):3520–3529.

    Article  Google Scholar 

Download references


We appreciated many undergraduate students from Heilongjiang Bayi Agricultural University for their help in field work.


This work was funded by Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23070103), National Natural Science Foundation of China (31822006 and 31770503), Youth Innovation Promotion Association CAS (Y201832), and Liaoning Revitalizing Talents Program (XLYC1807061).

Author information




XTL conceived the ideas. ZYL, GJY, YYH, ZWZ, SLH, and CD collected the data. ZYL, SS, and XTL analyzed the data. XTL and SS led the writing of the manuscript. All authors contributed critically to the drafts. The authors read and approved the final manuscript.

Corresponding author

Correspondence to Xiao-Tao Lü.

Ethics declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1 Table S1.

The number and identities of species being lost and gained in response to nitrogen addition under both unmown (control vs N) and mown (M vs NM) conditions in a temperate grassland. Figure S1. The N-induced changes of species loss and gain under unmown (a) and mown (b) conditions. Significance levels of the changes different from 0 were assessed using t-tests . *, P < 0.05; **, P < 0.01.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lü, XT., Liu, ZY., Sistla, S. et al. Linking changes of forage production and digestibility with grassland community assembly under nitrogen enrichment. Ecol Process 10, 33 (2021).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI:


  • Community composition
  • Nitrogen deposition
  • Species turnover
  • Price equation
  • Primary productivity