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Plant and Soil

, Volume 437, Issue 1–2, pp 455–471 | Cite as

Specific legumes allay drought effects on soil microbial food web activities of the focal species in agroecosystem

  • Feng Sun
  • Kaiwen PanEmail author
  • Olusanya Abiodun Olatunji
  • Zilong Li
  • Wenkai Chen
  • Aiping Zhang
  • Dagang Song
  • Xiaoming Sun
  • Dan Huang
  • Xue Tan
Regular Article

Abstract

Background and aims

The incidence of extreme weather events, particularly drought is predicted to increase in the future and alter the ecosystem process. Despite that the interplay between plant species play a critical role in reducing the vulnerability of soil ecosystem to drought, whether the presence of legumes in plant community could maintain nutrient uptake of focal species by stabilizing soil biota and ecosystem processes under drought conditions remains essentially unexplored.

Methods

In a field experiment, the soil biota community and ecosystem processes were studied using four planting systems contain monoculture of focal species Zanthoxylum bungeanum, mixed cultures of Z. bungeanum and Capsicum annuum, Z. bungeanum and Medicago sativa, and Z. bungeanum and Glycine max subjected to drought.

Results

Drought had no significant effects on soil microbial biomass in monoculture and mixed cultures, but significantly increased microbial stress indices. Drought significantly increased the densities of total nematodes, herbivores, bacterivores and fungivores in Z. bungeanum and M. sativa mixed culture, but significantly decreased the total nematodes, bacterivores and fungivores in Z. bungeanum and G. max mixed culture. Under drought stress, leaf nitrogen concentrations of Z. bungeanum were significantly higher in Z. bungeanum and M. sativa mixed culture than Z. bungeanum monoculture and the other mixed cultures, this is mainly due to higher microbial activity and net nitrogen mineralization rate.

Conclusion

Differences in resistance traits of neighbors had additive effects and rapidly reflected in different soil ecosystem processes and nutrient uptake of focal species. Our results revealed that specific legume species intercropping management could stabilize focal species by maintaining soil ecosystem processes under drought condition.

Keywords

Drought Agroforestry Zanthoxylum bungeanum Microorganisms Nematodes 

Notes

Acknowledgments

This study was supported by the National Key Research and Development Program of China (Grant Nos. 2016YFC0502101 and 2017YFC0505000), the National Natural Science Foundation of China (Grant Nos. 31370632, 31500517) and by the Ministry of Sciences and Technology of China (Grant No. 2015BAD07B050304).

References

  1. Arfin Khan MAS, Grant K, Beierkuhnlein C, Kreyling J, Jentsch A (2014) Climatic extremes lead to species-specific legume facilitation in an experimental temperate grassland. Plant Soil 379(1–2):161–175CrossRefGoogle Scholar
  2. Asuming-Brempong S, Gantner S, Adiku SGK, Archer G, Edusei V, Tiedje JM (2008) Changes in the biodiversity of microbial populations in tropical soils under different fallow treatments. Soil Biol Biochem 40(11):2811–2818CrossRefGoogle Scholar
  3. Bakonyi G, Nagy P, Kovács-Láng E, Kovács E, Barabás S, Répási V, Seres A (2007) Soil nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland. Appl Soil Ecol 37(1–2):31–40CrossRefGoogle Scholar
  4. Beauregard MS, Hamel C, Atul N, St-Arnaud M (2010) Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol 59(2):379–389CrossRefGoogle Scholar
  5. Bloor JMG, Bardgett RD (2012) Stability of above-ground and below-ground processes to extreme drought in model grassland ecosystems: interactions with plant species diversity and soil nitrogen availability. Perspect Plant Ecol 14(3):193–204CrossRefGoogle Scholar
  6. Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83(1):14–19CrossRefGoogle Scholar
  7. Borken W, Savage K, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Glob Chang Biol 12(2):177–193CrossRefGoogle Scholar
  8. Bossio D, Scow K (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278CrossRefGoogle Scholar
  9. Casida LE, Klein DA, Santoro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–378CrossRefGoogle Scholar
  10. Cesarz S, Reich PB, Scheu S, Ruess L, Schaefer M, Eisenhauer N (2015) Nematode functional guilds, not trophic groups, reflect shifts in soil food webs and processes in response to interacting global change factors. Pedobiologia 58(1):23–32CrossRefGoogle Scholar
  11. Chen LP, Zhao NX, Zhang LH, Gao YB (2013) Responses of two dominant plant species to drought stress and defoliation in the Inner Mongolia steppe of China. Plant Ecol 214:221–229CrossRefGoogle Scholar
  12. Dai A (2012) Increasing drought under global warming in observations and models. Nat Clim Chang 3(1):52–58CrossRefGoogle Scholar
  13. Daryanto S, Wang LX, Jacinthe PA (2017) Global synthesis of drought effects on cereal legume tuber and root crops production: a review. Agric Water Manag 179:18–33CrossRefGoogle Scholar
  14. de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265CrossRefGoogle Scholar
  15. de Vries FT, Liiri ME, Bjørnlund L, Setala HM, Christensen S, Bardgett RD (2012) Legacy effects of drought on plant growth and the soil food web. Oecologia 170(3):821–833CrossRefGoogle Scholar
  16. Dijkstra FA, Morgan JA, Blumenthal D, Follett RF (2010) Water limitation and plant inter-specific competition reduce rhizosphere-induced C decomposition and plant N uptake. Soil Biol Biochem 42(7):1073–1082CrossRefGoogle Scholar
  17. Eisenhauer N, Cesarz S, Koller R, Worm K, Reich PB (2012) Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity. Glob Chang Biol 18(2):435–447CrossRefGoogle Scholar
  18. Everard K, Seabloom EW, Harpole WS, de Mazancourt C (2010) Plant water use affects competition for nitrogen: why drought favors invasive species in California. Am Nat 175(1):85–97CrossRefGoogle Scholar
  19. Fenta BA, Beebe SE, Kunert KJ, Burridge JD, Barlow KM, Lynch JP, Foyer CH (2014) Field phenotyping of soybean roots for drought stress tolerance. Agronomy 4:418–435CrossRefGoogle Scholar
  20. Ferris H, Bongers T, de Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29CrossRefGoogle Scholar
  21. Frostegård A, Tunlid A, Bååth E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28:55–63CrossRefGoogle Scholar
  22. García-Orenes F, Guerrero C, Roldán A, Mataix-Solera J, Cerdà A, Campoy M, Zornoza R, Bárcenas G, Caravaca F (2010) Soil microbial biomass and activity under different agricultural management systems in a semiarid Mediterranean agroecosystem. Soil Tillage Res 109:110–115Google Scholar
  23. Görres JH, Savin MC, Neher DA, Weicht TR, Amador JA (1999) Grazing in a porous environment; The effect of soil pore structure on C. Plant Soil 212:75–83CrossRefGoogle Scholar
  24. Grant K, Kreyling J, Heilmeier H, Beierkuhnlein C, Jentsch A (2014) Extreme weather events and plant–plant interactions: shifts between competition and facilitation among grassland species in the face of drought and heavy rainfall. Ecol Res 29(5):991–1001CrossRefGoogle Scholar
  25. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37(2):112–129CrossRefGoogle Scholar
  26. Hamidi H, Safarnejad A (2010) Effect of drought stress on alfalfa cultivars (Medicago sativa L.) in germination stage. Am Eurasian J Agric Environ Sci 8(6):705–709Google Scholar
  27. Hartmann AA, Niklaus PA (2012) Effects of simulated drought and nitrogen fertilizer on plant productivity and nitrous oxide (N2O) emissions of two pastures. Plant Soil 361(1–2):411–426CrossRefGoogle Scholar
  28. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16(5):695–706CrossRefGoogle Scholar
  29. Huang X, Liu S, Wang H, Hu Z, Li Z, You Y (2014) Changes of soil microbial biomass carbon and community composition through mixing nitrogen fixing species with Eucalyptus urophyla in subtropical China. Soil Biol Biochem 73:42–48CrossRefGoogle Scholar
  30. IPCC (2012) Managing the risks of extreme events and. <World reference base for soil resources 2006.pdf>Google Scholar
  31. IUSS Working Group WRB (2007) World reference base forsoil resources 2006, first update 2007. World soilresources reports no. 103. FAO, RomeGoogle Scholar
  32. Jung V, Albert CH, Violle C, Kunstler G, Loucougaray G, Spiegelberger T, Cornwell W (2014) Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol 102(1):45–53CrossRefGoogle Scholar
  33. Kandeler E (1996) Protease activity. In: Schinner F, Ohlinger R, Kandeler E, Margesin R (eds) Methods in Soil Biology. Springer-Verlag, Berlin, pp 165–168Google Scholar
  34. Landesman WJ, Treonis AM, Dighton J (2011) Effects of a one-year rainfall manipulation on soil nematode abundances and community composition. Pedobiologia 54(2):87–91CrossRefGoogle Scholar
  35. Li H, Pan K, Liu Q, Wang J (2009) Effect of enhanced ultraviolet-B on allelopathic potential of Zanthoxylum bungeanum. Sci Hortic 119(3):310–314CrossRefGoogle Scholar
  36. Li D, Liu H, Qiao Y, Wang Y, Cai Z, Dong B, Shi C, Liu Y, Li X, Liu M (2013) Effects of elevated CO2 on the growth, seed yield, and water use efficiency of soybean (Glycine max (L.) Merr.) under drought stress. Agric Water Manag 129:105–112CrossRefGoogle Scholar
  37. Lv M, Shao Y, Lin Y, Liang C, Dai J, Liu Y, Fan P, Zhang W, Fu S (2016) Plants modify the effects of earthworms on the soil microbial community and its activity in a subtropical ecosystem. Soil Biol Biochem 103:446–451CrossRefGoogle Scholar
  38. Mariotte P, Robroek BJM, Jassey VEJ, Buttler A, Treseder K (2015) Subordinate plants mitigate drought effects on soil ecosystem processes by stimulating fungi. Funct Ecol 29(12):1578–1586CrossRefGoogle Scholar
  39. Mariotte P, Le Bayon RC, Eisenhauer N, Guenat C, Buttler A (2016) Subordinate plant species moderate drought effects on earthworm communities in grasslands. Soil Biol Biochem 96:119–127CrossRefGoogle Scholar
  40. Miller GL (1969) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428CrossRefGoogle Scholar
  41. Ng EL, Patti AF, Rose MT, Schefe CR, Smernik RJ, Cavagnaro TR (2015) Do organic inputs alter resistance and resilience of soil microbial community to drying? Soil Biol Biochem 81:58–66CrossRefGoogle Scholar
  42. Olatunji OA, Luo H, Pan K, Tariq A, Sun X, Chen W, Wu X, Zhang L, Xiong Q, Li Z, Song D, Zhang A, Sun F (2018a) Influence of phosphorus application and water deficit on the soil microbiota of N2-fixing and non-N-fixing tree. Ecosphere 9(6):e02276CrossRefGoogle Scholar
  43. Olatunji OA, Gong S, Tariq A, Pan K, Sun X, Chen W, Zhang L, Dakhil MA, Huang D, Tan X (2018b) The effect of phosphorus addition, soil moisture, and plant type on soil nematode abundance and community composition. J Soils Sediments.  https://doi.org/10.1007/s11368-018-2146-5
  44. Orwin KH, Wardle DA (2005) Plant species composition effects on belowground properties and the resistance and resilience of the soil microflora to a drying disturbance. Plant Soil 278(1–2):205–221CrossRefGoogle Scholar
  45. Pan K, Wang J, Lv K, Song L (2008) Effects of leaf leachates of Zanthoxylum bungeanum on soil enzymes, chemical properties and its own seedlings growth. Allelopath J 22(1):153–165Google Scholar
  46. Pan F, Li N, Zou WX, Han X, McLaughlin BN (2016) Soil nematode community structure and metabolic footprint in the early pedogenesis of a mollisol. Eur J Soil Biol 77:17–25Google Scholar
  47. Papatheodorou EM, Kordatos H, Kouseras T, Monokrousos N, Menkissoglu-Spiroudi U, Diamantopoulos J, Stamou GP, Argyropoulou MD (2012) Differential responses of structural and functional aspects of soil microbes and nematodes to abiotic and biotic modifications of the soil environment. Appl Soil Ecol 61:26–33CrossRefGoogle Scholar
  48. Pirhofer-Walzl K, Rasmussen J, Høgh-Jensen H, Eriksen J, Søegaard K, Rasmussen J (2012) Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant Soil 350(1–2):71–84CrossRefGoogle Scholar
  49. Sanaullah M, Blagodatskaya E, Chabbi A, Rumpel C, Kuzyakov Y (2011) Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Appl Soil Ecol 48(1):38–44CrossRefGoogle Scholar
  50. Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012) Carbon allocation in grassland communities under drought stress followed by 14C pulse labeling. Soil Biol Biochem 55:132–139CrossRefGoogle Scholar
  51. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394CrossRefGoogle Scholar
  52. Schinner F, von Mersi W (1990) Xylanase-, CM-cellulase- and invertase activity in soil: an improved method. Soil Biol Biochem 22(4):511–515Google Scholar
  53. Schoeneberger M, Bentrup G, de Gooijer H, Soolanayakanahally R, Sauer T, Brandle J, Zhou X, Current D (2012) Branching out: agroforestry as a climate change mitigation and adaptation tool for agriculture. J Soil Water Conserv 67(5):128–136CrossRefGoogle Scholar
  54. Shao Y, Wang X, Zhao J, Wu J, Zhang W, Neher DA, Li Y, Lou Y, Fu S (2016) Subordinate plants sustain the complexity and stability of soil micro-food webs in natural bamboo forest ecosystems. J Appl Ecol 53:130–139CrossRefGoogle Scholar
  55. Sun F, Pan K, Tariq A, Zhang L, Sun X, Li Z, Wang S, Xiong Q, Song D, Olatunji OA (2016a) The response of the soil microbial food web to extreme rainfall under different plant systems. Sci Rep 6:37662CrossRefGoogle Scholar
  56. Sun G, Wang Z, Zhu-Barker X, Zhang N, Wu N, Liu L, Lei Y (2016b) Biotic and abiotic controls in determining exceedingly variable responses of ecosystem functions to extreme seasonal precipitation in a mesophytic alpine grassland. Agric For Meteorol 228-229:180–190CrossRefGoogle Scholar
  57. Sun F, Pan K, Li Z, Wang S, Tariq A, Olatunji A, Sun X, Zhang L, Shi W, Wu X (2018) Soybean supplementation increases the resilience of microbial and nematode communities in soil toextreme rainfall in an agroforestry system. Sci Total Environ 626:776–784CrossRefGoogle Scholar
  58. Townshend J (1963) A modification and evaluation of the apparatus for the Oostenbrink direct cottonwool filter extraction method1. Nematologica 9(1):106–110CrossRefGoogle Scholar
  59. Wang JC, Pan KW, Wu N, Luo P, Li FH (2005) Effect of simplified agro-forest system of Sichuan pepper (Zanthoxylum avicennia) of some ecological factors. Chin J Appl Environ Biol 11:36–39Google Scholar
  60. Wang Z, Silva LCR, Sun G, Luo P, Mou C, Horwath WR (2014) Quantifying the impact of drought on soil-plant interactions: a seasonal analysis of biotic and abiotic controls of carbon and nutrient dynamics in high-altitudinal grasslands. Plant Soil 389(1–2):59–71Google Scholar
  61. Wang S, Pan K, Tariq A, Zhang L, Sun X, Li Z, Sun F, Xiong Q, Song D, Olatunji A (2018) Combined effects of cropping types and simulated extreme precipitation on the community composition and diversity of soil macrofauna in the eastern Qinghai-Tibet Plateau. J Soils Sediments 18:3215–3227CrossRefGoogle Scholar
  62. Whish JPM, Thompson JP, Clewett TG, Lawrence JL, Wood J (2014) Pratylenchus thornei populations reduce water uptake in intolerant wheat cultivars. Field Crop Res 161:1–10CrossRefGoogle Scholar
  63. Xu K, Yang D, Yang H, Li Z, Qin Y, Shen Y (2015) Spatio-temporal variation of drought in China during 1961–2012: a climatic perspective. J Hydrol 526:253–264CrossRefGoogle Scholar
  64. Yeates G, Bongers T, De Goede R, Freckman D, Georgieva S (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25(3):315–331Google Scholar
  65. Zhao J, Zeng ZX, He XY, Chen HS, Wang KL (2015) Effects of monoculture and mixed culture of grass and legume forage species on soil microbial community structure under different levels of nitrogen fertilization. Eur J Soil Biol 68:61–68CrossRefGoogle Scholar
  66. Zhou J, Sun X, Jiao J, Liu M, Hu F, Li H (2013) Dynamic changes of bacterial community under the influence of bacterial-feeding nematodes grazing in prometryne contaminated soil. Appl Soil Ecol 64:70–76CrossRefGoogle Scholar
  67. Zolla G, Badri DV, Bakker MG, Manter DK, Vivanco JM (2013) Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol 68:1–9CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of BiologyChinese Academy of SciencesChengduPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingPeople’s Republic of China

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