Biodiversity Science ›› 2018, Vol. 26 ›› Issue (12): 1296-1307.doi: 10.17520/biods.2018245

• Original Papers • Previous Article     Next Article

Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests

Yu Zhang1, Zhenggao Xiao1, Linhui Jiang1, Lei Qian2, Xiaoyun Chen1, Fajun Chen2, Feng Hu1, Manqiang Liu1, *()   

  1. 1 Soil Ecology Laboratory, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095
    2 College of Plant Protection, Nanjing Agricultural University, Nanjing 210095
  • Received:2018-09-12 Accepted:2018-11-19 Online:2019-02-11
  • Liu Manqiang
  • About author:# 同等贡献作者 Contributed equally to this work

Excessive chemical nitrogen (N) fertilizer application causes serious environmental problems and affects the ecosystem services that depend on soil biota. Earthworms improve soil fertility and plant productivity via activities such as feeding, burrowing and casting, and alter the relationships between crop plants and pests by modifying plant primary and secondary productivity. In order to mechanistically understand the functional roles of soil fauna in ecosystem services, a pot experiment using tomatoes (Lycopersicon esculentum) was conducted in a greenhouse. The study used a complete factorial design that manipulated earthworm (Metaphire guillelmi) abundance, western flower thrips (Frankliniella occidentalis) and N input. Results showed that under low N-input conditions, earthworms significantly reduced shoot and root biomass and shoot soluble sugar content, and increased shoot jasmonic acid content (by 6 times) and shoot salicylic acid content (by 3 times), compared to treatments without earthworms. This was accompanied by the decrease of thrips abundance by 58%, indicating a remarkable suppression of aboveground pests by earthworms. However, under high N-input conditions, earthworm presence did not affect the contents of shoot jasmonic acid or shoot salicylic acid or thrips abundance by the end of the experimental period (45 days). The earthworm-mediated responses of plant nutrition (shoot soluble sugar and shoot total nitrogen) was significantly positively correlated with thrips abundance, whereas defense (shoot jasmonic and salicylic acid) was significantly negatively correlated. Changes to soil N availability due to N fertilizer input can shift the direction of earthworm-mediated plant resistance against herbivores by altering plant resource acquisition and secondary defense. Effects of earthworms on plant growth and resistance depend on soil management practices such as N fertilizer application. A comprehensive understanding of the roles of soil biota in mediating plant growth requires knowledge of the multifaceted relationships among soil management, soil fauna, and plant pathogens.

Key words: soil fauna, plant chemistry, pests, aboveground-belowground, ecosystem service

Table 1

Changes in biomass and number of Metaphire guillelmi under different treatments"

接种时 Inoculation time 采样时 Sampling time 蚯蚓失重率
Weight loss of the earthworm (%)
数量 Number 生物量 Biomass (g) 数量 Number 生物量 Biomass (g)
低氮 Low N
高氮 High N
3 10.49 ± 0.27 3 9.19 ± 0.34 12.39
3 10.35 ± 0.24 3 8.63 ± 0.47 16.62
低氮 Low N
高氮 High N
3 10.19 ± 0.19 3 8.52 ± 0.22 16.39
3 10.27 ± 0.26 3 7.85 ± 0.66 23.56

Table 2

ANOVA results showing the effects of earthworm, nitrogen and herbivore on the contents of NO3--N, NH4+-N, microbial biomass carbon and microbial biomass nitrogen in soils"

变量 Variables 蚯蚓 Earthworm
(E) (df = 1)
氮素 Nitrogen
(N) (df = 1)
西花蓟马 Thrips
(WFT) (df = 1)
E × N
(df = 1)
(df = 1)
(df = 1)
E × N × WFT
(df = 1)
硝态氮 NO3--N 18.49*** 87.43*** 8.21** 18.02*** 3.51 6.67* 3.68
铵态氮 NH4+-N 4.07 2.06 10.82** 1.91 27.26*** 0.00 0.28
Microbial biomass carbon
10.35** 1.00 60.26*** 2.66 0.99 15.51*** 2.00
Microbial biomass nitrogen
11.94** 0.38 2.69 0.84 3.90 2.44 23.70***

Fig. 1

Effects of earthworm Metaphire guillelmi on the contents of soil NO3 --N, NH4+-N, microbial biomass carbon and microbial biomass nitrogen in the absence or presence of western flower thrips (WFT) under low and high N inputs (mean ± SD, n = 6). In the figure, -WFT and +WFT indicate without and with western flower thrips, respectively. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Table 3

Effects of earthworm, nitrogen, herbivore and their interactions on the nutrients and chemical traits of tomato shoots and roots"

蚯蚓 Earthworm
(E) (df = 1)
氮素 Nitrogen
(N) (df = 1)
西花蓟马 Thrips
(WFT) (df = 1)
E × N
(df = 1)
(df = 1)
(df = 1)
E × N × WFT
(df = 1)
茎叶干生物量 Shoot dry biomass 22.49*** 117.88*** 10.36** 2.39 1.64 5.86* 0.05
根系干生物量 Root dry biomass 13.77*** 2.08 0.20 11.47** 0.00 0.22 1.68
茎叶可溶性糖 Shoot soluble sugar 25.21*** 2.09 15.47*** 17.79*** 2.01 0.03 0.03
根系可溶性糖 Root soluble sugar 0.01 0.71 2.68 2.17 3.69 1.39 13.09***
茎叶全氮 Shoot total nitrogen 12.21** 182.83*** 1.19 3.10 0.00 0.07 1.70
根系全氮 Root total nitrogen 20.37*** 246.77*** 15.21*** 0.06 11.12** 2.79 2.11
茎叶游离氨基酸 Shoot amino acid 0.97 20.43*** 7.57** 0.73 0.28 26.10*** 8.31**
根系游离氨基酸 Root amino acid 46.10*** 43.08*** 7.38** 21.88*** 14.80*** 32.87*** 0.96
茎叶酚 Shoot phenolics 2.36 36.23*** 4.75* 1.50 2.26 0.31 29.01***
根系酚 Root phenolics 3.61 0.01 51.47*** 9.75** 0.00 0.01 33.56***
茎叶水杨酸 Shoot salicylic acid 49.52*** 0.08 0.11 72.61*** 80.09*** 18.73*** 95.11***
茎叶茉莉酸 Shoot jasmonic acid 156.85*** 3.54 26.94*** 38.62*** 83.52*** 64.95*** 116.73***

Fig. 2

Effects of earthworm Metaphire guillelmi on the contents of tomato shoot dry biomass, root dry biomass, shoot soluble sugar, root soluble sugar, shoot amino acid, root amino acid, shoot total nitrogen and root total nitrogen in the absence or presence of western flower thrips under low and high N inputs (mean ± SD, n = 6). In the figure, -WFT and +WFT indicate without and with western flower thrips, respectively. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Fig. 3

Effects of earthworm Metaphire guillelmi on the contents of tomato shoot phenolics, root phenolics, shoot jasmonic acid and shoot salicylic acid in the absence or presence of western flower thrips (WFT) under low and high N inputs (mean ± SD, n = 6). In the figure, -WFT and +WFT indicate without and with western flower thrips, respectively. Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Fig. 4

Effects of earthworm and nitrogen level on the abundance of western flower thrips (WFT) (mean ± SD, n = 6). Means with different letters indicate significant difference among treatments (Fisher’s LSD test, P < 0.05). Error bars are standard errors."

Fig. 5

Regressions between western flower thrips (WFT) abundance and contents of tomato shoot soluble sugar, shoot total nitrogen, shoot salicylic acid and shoot jasmonic acid."

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