Sciences in Cold and Arid Regions ›› 2018, Vol. 10 ›› Issue (4): 293-304.doi: 10.3724/SP.J.1226.2018.00293

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Biodiversity, productivity, and temporal stability in a natural grassland ecosystem of China

Bing Liu*(),WenZhi Zhao,YangYang Meng,Chan Liu   

  1. Linze Inland River Basin Research Station, Key Laboratory of Ecohydrology of Inland River Basin, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences, Lanzhou, Gansu 730000, China
  • Received:2018-01-26 Accepted:2018-05-12 Online:2018-08-01 Published:2018-11-22
  • Contact: Bing Liu E-mail:liubing@lzb.ac.cn
  • Supported by:
    This study was supported by the National Basic Research Program of China (No. 2013CB429903), and the National Natural Science Foundation of China (Nos. 41471024; 41771038). We thank all participants in the vegetation and environmental surveys at the Forestry Bureau of Yanchi County, Ningxia Hui Autonomous Region, China.

Abstract:

Understanding the effect of biodiversity on ecosystem function is critical to promoting the sustainability of ecosystems and species conservation in natural ecosystems. We observed species composition, species richness and aboveground biomass, and simulated the competitive assemblages in a natural grassland ecosystem of China, aiming to test some assumptions and predictions about biodiversity–stability relationships. Our results show that aboveground productivity and temporal stability increased significantly with increasing species richness, and via a combination of overyielding, species asynchrony, and portfolio effects. Species interactions resulted in overyielding caused by trait-independent complementarity, and were not offset by a negative dominance effect and trait-dependent complementarity effect. Therefore, the mechanisms underlying the biodiversity effect shifted from the selection effect to the complementarity effect as diversity increased, and both effects were coexisted but the complementarity effect represent a mechanism that facilitates long term species coexistence in a natural grassland ecosystem of China.

Key words: biodiversity, productivity, temporal stability, overyielding effect, species interactions, complementarity effect, selection effect

Figure 1

Relationships between species richness and (a) aboveground productivity, (b) temporal stability, and (c) community-wide synchrony. Means for a parameter (± SEM) labelled with different letters differ significantly (Tukey's HSD; ***, P <0.001; **, P <0.01; *, P <0.05) "

Table 1

Summary of the statistical results for productivity, community stability, and species synchrony, as well as their interactions with the key species variables"

Item d.f. Productivity Community stability Species synchrony
MS F P MS F P MS F P
Species richness (SR) 5,120 11,693.51 97.38*** 0.001 15.64 7.46* 0.028 14.72 6.30*** 0.001
Functional group number (FG) 2,98 8,991.22 7.57* 0.019 13.42 5.45* 0.038 16.67 5.05* 0.038
Species ID 21,132 10,138.33 2.96*** < 0.001 10.10 0.83 0.68 19.03 1.25 0.220
Annual herbs 20,132 4,334.50 1.08 0.354 0.16 0.03 0.973 76.29 2.37 0.111
Perennial herbs 34,121 15,494.79 4.46* 0.020 1.48 0.52 0.599 2.21 1.99 0.169
Subshrubs 7,133 3,755.39 1.38 0.267 58.72 1.55 0.230 29.32 0.49 0.620
SR × FG 11,136 5,044.74 5.44* 0.016 2.49 0.20 0.996 6.42 0.41 0.942
Species ID × SR 5,128 386.37 2.42* 0.045 31,043.93 10.50*** < 0.001 18.55 1.57 0.184
Annual herbs × SR 6,131 522.44 0.14 0.988 3.03 0.69 0.657 8.40 1.29 0.935
Perennial herbs × SR 5,128 3,295.73 12.66*** 0.001 2.03 0.69 0.423 2.03 1.03 0.957
Subshrubs × SR 4,124 5,933.25 1.69 0.155 4.35 0.27 0.893 1.15 0.07 0.989
Species ID × Annual herbs 3,117 693.681 0.17* 0.013 10.79 2.63 0.080 8.47 0.29 0.830
Species ID × Perennial herbs 5,128 3,712.13 13.39*** 0.001 1.145 0.36 0.867 0.71 0.38 0.853
Species ID × Subshrubs 8,134 1,688.099 1.63 0.751 15.26 1.45 0.236 0.16 0.33 0.947

Figure 2

Effects of plant diversity on the relationship between community-wide synchrony and its temporal stability. (a) 2 species, (b) 5 species, (c) 10 species, (d) 15 species, (e) 20 species"

Figure 3

Effects of species richness on (a) the relative yield total (RYT), (b) the net effect, (c) the complementarity effect, and (d) the selection effect. Means ± SEM labelled with different letters differ significantly (Tukey's HSD, P <0.05) "

Table 2

Summary of the analysis of net biodiversity effects, the two components of the complementarity effect, and the selection effect"

Item d.f. Net effect (ΔY) Complementarity effect ( $N\overline {\Delta \!{\textit {R\!Y}}}\! \times \overline {\textit \!{M}} $ ) Selection effect
(N cov(ΔRY, M))
MS F P MS F P MS F P
Species richness (SR) 4,207 2,522.85 38.03*** < 0.001 4,786.07 46.86*** < 0.001 526.93 13.33*** < 0.001
Functional group number (FG) 2,207 300.77 4.53** 0.002 365.08 3.57** 0.009 37.94 0.96 0.433
Species ID 23,208 70.27 1.06 0.403 130.25 1.28 0.204 51.93 1.31 0.178
SR × FG 8,208 123.30 1.90 0.075 106.20 1.00 0.411 22.40 0.60 0.802
SR × Species ID 34,208 102.70 1.55* 0.049 105.19 1.03 0.440 44.66 1.13 0.314
FG × Species ID 21,208 77.27 1.16 0.298 52.25 0.51 0.960 31.62 0.80 0.714
SR × FG × Species ID 7,208 64.27 0.97 0.458 280.37 2.74** 0.012 159.41 4.03*** 0.001

Figure 4

Interactions that influenced temporal stability. (a) the complementarity effect and (b) the selection effect"

Figure 5

Comparison of the measured and simulated values of the (a–c) trait-independent complementarity (TIC), (d–f) trait-dependent complementarity (TDC), (g–i) dominance effect (DE), and (j–l) net biodiversity effect (ΔY) in neutral, dominant and trade-off communities "

Table 3

Statistical summaries of measured and simulated parameters in the neutral, dominant, and trade-off communities"

Item Measured Simulated
Neutral Dominant Trade-off
TIC 7.75 ± 1.81a 1.18 ± 1.23d 5.33 ± 1.36b 2.90 ± 1.51c
TDC ?0.25 ± 0.18b ?0.01 ± 0.09b 0.61 ± 0.09a ?0.68 ± 0.10c
DE ?0.01 ± 0.01b 0.00 ± 0.00b 0.03 ± 0.00a ?0.03 ± 0.01c
ΔY 10.24 ± 1.26a 1.76 ± 0.97c 7.60 ± 1.18b 0.89 ± 1.32d

Figure 6

Effects of species richness on the (a) trait-independent complementarity (TIC), (b) trait-dependent complementarity (TDC), and (c) dominance effect (DE) in neutral, dominant and trade-off communities "

1 Bai YF, Han XG, Wu JG, et al. Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 2004; 431: 7005 181- 184.
doi: 10.1038/nature02850
2 Bond EM, Chase JM Biodiversity and ecosystem functioning at local and regional spatial scales. Ecology Letters 2002; 5: 4 467- 470.
doi: 10.1046/j.1461-0248.2002.00350.x
3 Bruno JF, Boyer KE, Duffy JE, et al. Effects of macroalgal species identity and richness on primary production in benthic marine communities. Ecology Letters 2005; 8: 11 1165- 1174.
doi: 10.1111/j.1461-0248.2005.00823.x
4 Butler AJ From populations to ecosystems: theoretical foundations for a new ecological synthesis. Austral Ecology 2011; 36: 8 e53- e54.
doi: 10.1111/j.1442-9993.2011.02326.x
5 Chase JM Stochastic community assembly causes higher biodiversity in more productive environments. Science 2010; 328: 5984 1388- 1391.
doi: 10.1126/science.1187820
6 Cottingham KL, Brown BL, Lennon JT Biodiversity may regulate the temporal variability of ecological systems. Ecology Letters 2001; 4: 1 72- 85.
doi: 10.1046/j.1461-0248.2001.00189.x
7 De Mazancourt C, Isbell F, Larocque A, et al. Predicting ecosystem stability from community composition and biodiversity. Ecology Letters 2013; 16: 5 617- 625.
doi: 10.1111/ele.12088
8 Fargione J, Tilman D, Dybzinski R, et al. From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proceedings of the Royal Society B: Biological Sciences 2007; 274: 1611 871- 876.
doi: 10.1098/rspb.2006.0351
9 Fowler MS, Laakso J, Kaitala V, et al. Species dynamics alter community diversity–biomass stability relationships. Ecology Letters 2012; 15: 12 1387- 1396.
doi: 10.1111/j.1461-0248.2012.01862.x
10 Fox JW Interpreting the 'selection effect' of biodiversity on ecosystem function. Ecology Letters 2005; 8: 8 846- 856.
doi: 10.1111/j.1461-0248.2005.00795.x
11 Fridley JD The influence of species diversity on ecosystem productivity: how, where, and why?. Oikos 2001; 93: 3 514- 526.
doi: 10.1034/j.1600-0706.2001.930318.x
12 Gamfeldt L, Snäll T, Bagchi R, et al. Higher levels of multiple ecosystem services are found in forests with more tree species. Nature Communications 2013; 4: 1 1340.
doi: 10.1038/ncomms2328
13 Gonzalez A, Loreau M The causes and consequences of compensatory dynamics in ecological communities. Annual Review of Ecology, Evolution, and Systematics 2009; 40: 393- 414.
doi: 10.1146/annurev.ecolsys.39.110707.173349
14 Grime JP Plant strategies, vegetation processes, and ecosystem properties. Journal of Vegetation Science 2002; 13: 2 294- 295.
doi: 10.1658/1100-9233(2002)013[0294:PSVPAE]2.0.CO;2
15 Haddad NM, Crutsinger GM, Gross K, et al. Plant diversity and the stability of foodwebs. Ecology Letters 2011; 14: 1 42- 46.
doi: 10.1111/j.1461-0248.2010.01548.x
16 Hautier Y, Seabloom EW, Borer ET, et al. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 2014; 508: 7497 521- 525.
doi: 10.1038/nature13014
17 Hector A, Schmid B, Beierkuhnlein C, et al. Plant diversity and productivity experiments in European grasslands. Science 1999; 286: 5442 1123- 1127.
doi: 10.1126/science.286.5442.1123
18 Hector A, Hautier Y, Saner P, et al. General stabilizing effects of plant diversity on grassland productivity through population asynchrony and overyielding. Ecology 2010; 91: 8 2213- 2220.
doi: 10.1890/09-1162.1
19 Hooper DU, Vitousek PM The effects of plant composition and diversity on ecosystem processes. Science 1997; 277: 5330 1302- 1305.
doi: 10.1126/science.277.5330.1302
20 Hooper DU, Dukes JS Overyielding among plant functional groups in a long-term experiment. Ecology Letters 2004; 7: 2 95- 105.
doi: 10.1046/j.1461-0248.2003.00555.x
21 Hooper DU, Adair EC, Cardinale BJ, et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 2012; 486: 7401 105- 108.
doi: 10.1038/nature11118
22 Huston MA, Aarssen LW, Austin MP, et al. No consistent effect of plant diversity on productivity. Science 2000; 289: 5483 1255.
doi: 10.1126/science.289.5483.1255a
23 Isbell FI, Polley HW, Wilsey BJ Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecology Letters 2009; 12: 5 443- 451.
doi: 10.1111/j.1461-0248.2009.01299.x
24 Ives AR, Carpenter SR Stability and diversity of ecosystems. Science 2007; 317: 5834 58- 62.
doi: 10.1126/science.1133258
25 Jucker T, Bouriaud O, Avacaritei D, et al. Stabilizing effects of diversity on aboveground wood production in forest ecosystems: linking patterns and processes. Ecology Letters 2014; 17: 12 1560- 1569.
doi: 10.1111/ele.12382
26 Lehman CL, Tilman D Biodiversity, stability, and productivity in competitive communities. The American Naturalist 2000; 156: 5 534- 552.
doi: 10.1086/303402
27 Liu B, Zhao WZ, Liu ZL, et al. Changes in species diversity, aboveground biomass, and vegetation cover along an afforestation successional gradient in a semiarid desert steppe of China. Ecological Engineering 2015; 81: 301- 311.
doi: 10.1016/j.ecoleng.2015.04.014
28 Long ZT, Bruno JF, Duffy JE Biodiversity mediates productivity through different mechanisms at adjacent trophic levels. Ecology 2007; 88: 11 2821- 2829.
doi: 10.1890/06-1977.1
29 Loreau M Biodiversity and ecosystem functioning: a mechanistic model. Proceedings of the National Academy of Sciences of the United States of America 1998; 95: 10 5632- 5636.
doi: 10.1073/pnas.95.10.5632
30 Loreau M, Hector A Partitioning selection and complementarity in biodiversity experiments. Nature 2001; 412: 6842 72- 76.
doi: 10.1038/35083573
31 Loreau M, de Mazancourt C Species synchrony and its drivers: neutral and nonneutral community dynamics in fluctuating environments. The American Naturalist 2008; 172: 2 48- 66.
doi: 10.1086/589746
32 Loreau M, de Mazancourt C Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecology letters 2013; 16: S1 106- 115.
doi: 10.1111/ele.12073
33 McCann KS The diversity-stability debate. Nature 2000; 405: 6783 228- 233.
doi: 10.1038/35012234
34 Morin X, Fahse L, de Mazancourt C, et al. Temporal stability in forest productivity increases with tree diversity due to asynchrony in species dynamics. Ecology Letters 2014; 17: 12 1526- 1535.
doi: 10.1111/ele.12357
35 Naeem S, Thompson LJ, Lawler SP, et al. Declining biodiversity can alter the performance of ecosystems. Nature 1994; 368: 6473 734- 737.
doi: 10.1038/368734a0
36 Polley HW, Wilsey BJ, Derner JD Do species evenness and plant density influence the magnitude of selection and complementarity effects in annual plant species mixtures?. Ecology Letters 2003; 6: 3 248- 256.
doi: 10.1046/j.1461-0248.2003.00422.x
37 Polley HW, Wilsey BJ, Derner JD Dominant species constrain effects of species diversity on temporal variability in biomass production of tallgrass prairie. Oikos 2007; 116: 12 2044- 2052.
doi: 10.1111/j.2007.0030-1299.16080.x
38 Rees M, Condit R, Crawley M, et al. Long-term studies of vegetation dynamics. Science 2001; 293: 5530 650- 655.
doi: 10.1126/science.1062586
39 Roscher C, Weigelt A, Proulx R, et al. Identifying population- and community-level mechanisms of diversity–stability relationships in experimental grasslands. Journal of Ecology 2011; 99: 6 1460- 1469.
doi: 10.1111/j.1365-2745.2011.01875.x
40 Steiner CF, Long ZT, Krumins JA, et al. Temporal stability of aquatic food webs: partitioning the effects of species diversity, species composition and enrichment. Ecology Letters 2005; 8: 8 819- 828.
doi: 10.1111/j.1461-0248.2005.00785.x
41 Tilman D, Wedin D, Knops J Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 1996; 379: 6567 718- 720.
doi: 10.1038/379718a0
42 Tilman D The ecological consequences of changes in biodiversity: a search for general principles. Ecology 1999; 80: 5 1455- 1474.
doi: 10.1890/0012-9658(1999)080[1455:TECOCI]2.0.CO;2
43 Tilman D, Reich PB, Knops J, et al. Diversity and productivity in a long-term grassland experiment. Science 2001; 294: 5543 843- 845.
doi: 10.1126/science.1060391
44 Tilman D, Reich PB, Johannes, et al. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 2006; 441: 7093 629- 632.
doi: 10.1038/nature04742
45 Valone TJ, Schutzenhofer MR Reduced rodent biodiversity destabilizes plant populations. Ecology 2007; 88: 1 26- 31.
doi: 10.1890/0012-9658(2007)88[26:RRBDPP]2.0.CO;2
46 Van Ruijven J, Berendse F Positive effects of plant species diversity on productivity in the absence of legumes. Ecology Letters 2003; 6: 3 170- 175.
doi: 10.1046/j.1461-0248.2003.00427.x
47 Van Ruijven J, Berendse F Diversity–productivity relationships: initial effects, long-term patterns, and underlying mechanisms. Proceedings of the National Academy of Sciences of the United States of America 2005; 102: 3 695- 700.
doi: 10.1073/pnas.0407524102
48 Van Ruijven J, Berendse F Contrasting effects of diversity on the temporal stability of plant populations. Oikos 2007; 116: 8 1323- 1330.
doi: 10.1111/j.0030-1299.2007.16005.x
49 Worm B, Duffy JE Biodiversity, productivity and stability in real food webs. Trends in Ecology & Evolution 2003; 18: 12 628- 632.
doi: 10.1016/j.tree.2003.09.003
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