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

doi:10.17520/biods.2018245

Abstract

Abstract:

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.

http://jtp.cnki.net/bilingual/detail/html/SWDY201812005

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

Yu Zhang, Zhenggao Xiao, Linhui Jiang, Lei Qian, Xiaoyun Chen, Fajun Chen, Feng Hu, Manqiang Liu. Nitrogen levels modify earthworm-mediated tomato growth and resistance to pests[J]. Biodiv Sci, 2018, 26(12): 1296-1307.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2018245

https://www.biodiversity-science.net/EN/Y2018/V26/I12/1296

Figures/Tables 8

Table 1 Changes in biomass and number of Metaphire guillelmi under different treatments

处理 Treatments		接种时 Inoculation time		采样时 Sampling time		蚯蚓失重率 Weight loss of the earthworm (%)
处理 Treatments		数量 Number	生物量 Biomass (g)	数量 Number	生物量 Biomass (g)	蚯蚓失重率 Weight loss of the earthworm (%)
无西花蓟马 -WFT	低氮 Low N 高氮 High N	3	10.49 ± 0.27	3	9.19 ± 0.34	12.39
无西花蓟马 -WFT	低氮 Low N 高氮 High N	3	10.35 ± 0.24	3	8.63 ± 0.47	16.62
接种西花蓟马 +WFT	低氮 Low N 高氮 High N	3	10.19 ± 0.19	3	8.52 ± 0.22	16.39
接种西花蓟马 +WFT	低氮 Low N 高氮 High N	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)	E × WFT (df = 1)	N × WFT (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
微生物生物量碳 Microbial biomass carbon	10.35^**	1.00	60.26^***	2.66	0.99	15.51^***	2.00
微生物生物量氮 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

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)	E × WFT (df = 1)	N × WFT (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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