Latitude distribution and associated environmental factors of soil nematodes in a typical black soil region

doi:10.17520/biods.2022269

Abstract

Abstract:

Aims: Northeast black soil is one of the most important agricultural resources in China. Understanding the spatial distribution of nematode communities as well as their influcing factors is of great importance for ensuring food security in China.
Methods: In September 2018, 31 farmland sampling sites were selected across the black soil region within the bounds of 42°50°-49°08° N, and 93 soil samples were collected. Soil nematode communities were identified by morphological identification.
Results: A total of 47 nematode genera (relative abundance > 1%) were identified. Across all samples, the bacterivores nematode Acrobloides was the most abundant (relative abundance > 5%). Species richness and abundance of nematode communities increased with latitude, but only among bacterivores and omnivores/predators nematodes. Soil organic carbon was the most important environmental factor affecting richness and abundance of soil nematodes in a typical black soil region, followed by monthly mean temperature. Soil nematode community structure in this region was divided into two categories: south and north, with a boundary at 47° N separating the two groups. This division was attributed mainly to the differences in the relative abundance of plant parasitic and omnivorous/predatory nematodes between the two areas. Soil pH value and bulk density were the most important factors influencing community structure in the south and north, respectively.
Conclusion: This study clarifies the relationship between environmental factors and nematode community structure, as well the geographical distribution of nematode communities in a typical black soil region. As such, it provides basic data and reference for the mechanism driving the character of soil biota under agricultural interference.

Key words: black soil, nematodes, latitude, driving factors, soil organic carbon

Ping Liu, Hongwen Liu, Miao Zhang, Yan Gao, Mengting Zhang, Aizhen Liang, Shixiu Zhang. Latitude distribution and associated environmental factors of soil nematodes in a typical black soil region[J]. Biodiv Sci, 2022, 30(12): 22269.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2022269

https://www.biodiversity-science.net/EN/Y2022/V30/I12/22269

Figures/Tables 6

Fig. 1 Distribution of 23 farmland sample plots with corn in the typical black soil region

Fig. 2 The relationship between latitude and the richness (a-e) and abundance (f-j) of soil nematodes community in farmland of the typical black soil region. The shaded areas are 95% confidence intervals.

Table 1 The importance ranking of environmental factors affecting soil nematode richness and abundance in the typical black soil region

丰富度 Richness	环境因子 Environmental factors	%IncMSE	显著性 Significance	多度 Abundance	环境因子 Environmental factors	%IncMSE	显著性 Significance
Total R	SOC	8.76	**	Total A	SOC	8.53	**
	pH	8.23	*		MMR	6.21	*
	MMT	6.52	*		MMT	5.59	*
Ba R	SOC	12.58	**	Ba A	SOC	9.42	**
	pH	11.98	**		MMR	6.50	*
	MMT	8.73	**		MMT	5.40
PP R	MMT	6.83	*	Fu A	CC	8.38	**
	SOC	3.48			MMR	6.29	*
	SBD	2.90			MMT	4.94
OP R	MMT	8.42	**	OP A	SOC	9.53	**
	SOC	7.68	**		SM	5.71
	DOC	6.99	*		pH	4.80

Fig. 3 Differential response map of soil nematode community in the typical black soil region. A, Cluster analysis of soil nematode community in farmland of the typical black soil region; B, Characteristic genus of soil nematodes in northern and southern typical black soil regions (likelihood ratio test, P < 0.05, FDR corrected). The name of characteristic genus and their c-p values were listed in the adjacent red and blue dashed line boxes on the right. Ba, Bacterivores; Fu, Fungivores; PP, Plant parasites; OP, Omnivores/predators; South, Nematode community of southern characteristic genus; None, Nematode community with no statistical difference; North, Nematode community of northern characteristic genus. CT1, Changtu1; CT2, Changtu2; LS1, Lishu1; LS2, Lishu2; GZL, Gongzhuling; CC1, Changchun; DH, Dehui; YS, Yushu; SC, Shuangcheng; HEB, Harbin; HL1, Hulan; BY, Bayan; SH, Suihua; SL, Suileng; HL, Hailun; BQ, Baiquan; BA, Bei’an; KD, Kedong; NH1, Nehe1; NH2, Nehe2; WDLC1, Wudalianchi1; WDLC2, Wudalianchi2; NJ, Nenjiang.

Fig. 4 Box plot of the relative abundance of soil nematode trophic groups in the typical black soil region. A, Differences in the relative abundance of trophic groups of overall nematode community between southern and northern typical black soil regions; B, Differences in the relative abundance of trophic groups of soil nematode characteristic genera community between southern and northern typical black soil regions. S13 represents 13 samples in the south, and N10 represents 10 samples in the north. Ba, Bacterivores; Fu, Fungivores; PP, Plant parasites; OP, Omnivores/predators.

Table 2 The importance ranking of environmental factors affecting the nematode and characteristic genus community structure in southern and northern typical black soil regions

线虫群落结构 Nematode community structure	环境因子 Environmental factors	%IncMSE	显著性 Significance	特征属线虫群落结构 Characteristic genus community structure	环境因子 Environmental factors	%IncMSE	显著性 Significance
南部13个样点 13 samples in the south (S13)	pH	11.73	**	S13	CC	15.36	**
	CC	10.68	**		pH	12.30	**
	DOC	10.49	**		SOC	11.11	**
北部10个样点 10 samples in the north (N10)	SBD	13.04	**	N10	MMT	14.20	**
	SOC	12.65	**		SBD	13.07	**
	pH	9.42	**		MMR	11.57	**

References 48

[1]	Bongers T (1988) De Nematoden Van Nederland. Stichting Uitgeverij Koninklijke Nederlandse Natuurhistorische Vereniging, Utrecht. (in Dutch)
[2]	Bongers T (1990) The maturity index: An ecological measure of environmental disturbance based on nematode species composition. Oecologia, 83, 14-19. DOI PMID
[3]	Bongers T, Bongers M (1998) Functional diversity of nematodes. Applied Soil Ecology, 10, 239-251. DOI URL
[4]	Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology & Evolution, 14, 224-228. DOI URL
[5]	Chan KY (1981) Representative sampling for bulk density in a vertisol. Soil Science Society of America Journal, 45, 668-669. DOI URL
[6]	da Rocha MR, de Carvalho Y, Cattini GP, Paolini G (2006) Efeito de doses crescentes de calcário sobre a população de Heterodera glycines em soja. Pesquisa Agropecuária Tropical, 36, 89-94. (in Portuguese)
[7]	De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos, 119, 1674-1684. DOI URL
[8]	Du Preez G, Daneel M, De Goede R, Du Toit MJ, Ferris H, Fourie H, Geisen S, Kakouli-Duarte T, Korthals G, Sánchez-Moreno S, Schmidt JH (2022) Nematode-based indices in soil ecology: Application, utility, and future directions. Soil Biology and Biochemistry, 169, 108640. DOI URL
[9]	Ferris H, Bongers T (2009) Indices developed specifically for analysis of nematode assemblages. In: Nematodesas Environmental Indicators (WilsonMJ,eds Kakouli-Duarte T), pp. 124-145. CAB International, London.
[10]	Ferris H, Bongers T,de Goede RGM (2001) A framework for soil food web diagnostics: Extension of the nematode faunal analysis concept. Applied Soil Ecology, 18, 13-29. DOI URL
[11]	Fu SL, Zhang WX, Shao YH, Shi LL, Zhang X, Shi NN, Zhao CC, Zhang CL, Liu ZF, Mao P, Lin YB, Yu SQ, Cao JB, Sun F, Xu GL, Zhao J, Wu JP, Liu SJ, Wang XL, Sun YX, Fang YT, Wan SZ (2019) Soil Ecology:Soil Food Web and Its Ecological Functions. Science Press, Beijing. (in Chinese)
	[ 傅声雷, 张卫信, 邵元虎, 时雷雷, 张晓, 史楠楠, 赵灿灿, 张晨露, 刘占峰, 毛鹏, 林永标, 余世钦, 曹建波, 孙峰, 徐国良, 赵杰, 吴建平, 刘胜杰, 王晓丽, 孙毓鑫, 方运霆, 万松泽 (2019) 土壤生态学——土壤食物网及其生态功能. 科学出版社, 北京.]
[12]	Grömping U (2009) Variable importance assessment in regression: Linear regression versus random forest. The American Statistician, 63, 308-319. DOI URL
[13]	Guo XH, Endler A, Poll C, Marhan S, Ruess L (2021) Independent effects of warming and altered precipitation pattern on nematode community structure in an arable field. Agriculture, Ecosystems and Environment, 316, 107467. DOI URL
[14]	Hartman K, van der Heijden MGA, Wittwer RA, Banerjee S, Walser JC, Schlaeppi K (2018) Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome, 6, 74. DOI PMID
[15]	Hua E, Sun YT, Zhang ZN, He L, Cui CY, Mu FH (2019) Effects of reduced seawater pH on nematode community composition and diversity in sandy sediments. Marine Environmental Research, 150, 104773. DOI URL
[16]	Hunt HW, Wall DH (2002) Modelling the effects of loss of soil biodiversity on ecosystem function. Global Change Biology, 8, 33-50. DOI URL
[17]	Karuri H (2022) Root and soil health management approaches for control of plant parasitic nematodes in sub-Saharan Africa. Crop Protection, 152, 105841. DOI URL
[18]	Korthals GW, Bongers T, Kammenga JE, Alexiev AD, Lexmond TM (1996) Long-term effects of copper and pH on the nematode community in an agroecosystem. Environmental Toxicology and Chemistry, 15, 979-985. DOI URL
[19]	Lee MR, Riveros M (2012) Latitudinal trends in the species richness of free-living marine nematode assemblages from exposed sandy beaches along the coast of Chile (18-42° S). Marine Ecology, 33, 317-325. DOI URL
[20]	Li Q (2017) Soil Nematodes of Grasslands in Northern China. Elsevier, Amsterdam.
[21]	Li XP, Zhu HM, Geisen S, Bellard C, Hu F, Li HX, Chen XY, Liu MQ (2020) Agriculture erases climate constraints on soil nematode communities across large spatial scales. Global Change Biology, 26, 919-930. DOI PMID
[22]	Liang WJ, Lou YL, Li Q, Zhong S, Zhang XK, Wang JK (2009) Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biology and Biochemistry, 41, 883-890. DOI URL
[23]	Liu JJ, Sui YY, Yu ZH, Shi Y, Chu HY, Jin J, Liu XB, Wang GH (2014) High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of Northeast China. Soil Biology and Biochemistry, 70, 113-122. DOI URL
[24]	Liu T, Hu F, Li HX (2019) Spatial ecology of soil nematodes: Perspectives from global to micro scales. Soil Biology and Biochemistry, 137, 107565. DOI URL
[25]	Liu YB, Zhang GL, Xie Y, Shen B, Gu ZJ, Ding YY (2021) Delineating the black soil region and typical black soil region of northeastern China. Chinese Science Bulletin, 66, 96-106. (in Chinese with English abstract)
	[ 刘宝元, 张甘霖, 谢云, 沈波, 顾治家, 丁迎盈 (2021) 东北黑土区和东北典型黑土区的范围与划界. 科学通报, 66, 96-106.]
[26]	Mueller KE, Blumenthal DM, Carrillo Y, Cesarz S, Ciobanu M, Hines J, Pabst S, Pendall E, de Tomasel M, Wall DH, Eisenhauer N (2016) Elevated CO₂ and warming shift the functional composition of soil nematode communities in a semiarid grassland. Soil Biology and Biochemistry, 103, 46-51. DOI URL
[27]	Pan FJ, Xu YL, McLaughlin NB, Xue AG, Yu Q, Han XZ, Liu W, Zhan LL, Zhao D, Li CJ (2012) Response of soil nematode community structure and diversity to long-term land use in the black soil region in China. Ecological Research, 27, 701-714. DOI URL
[28]	Quist CW, Gort G, Mooijman P, Brus DJ, van den Elsen S, Kostenko O, Vervoort M, Bakker J, van der Putten WH, Helder J (2019) Spatial distribution of soil nematodes relates to soil organic matter and life strategy. Soil Biology and Biochemistry, 136, 107542. DOI URL
[29]	Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140. DOI PMID
[30]	Sánchez-Moreno S, Ferris H, Young-Mathews A, Culman SW, Jackson LE (2011) Abundance, diversity and connectance of soil food web channels along environmental gradients in an agricultural landscape. Soil Biology and Biochemistry, 43, 2374-2383. DOI URL
[31]	Shao YH, Fu SL (2007) The diversity and functions of soil nematodes. Biodiversity Science, 15, 116-123. (in Chinese with English abstract) DOI
	[ 邵元虎, 傅声雷 (2007) 试论土壤线虫多样性在生态系统中的作用. 生物多样性, 15, 116-123.] DOI
[32]	Sechi V, de Goede RGM, Rutgers M, Brussaard L, Mulder C (2018) Functional diversity in nematode communities across terrestrial ecosystems. Basic and Applied Ecology, 30, 76-86. DOI URL
[33]	Serna-Chavez HM, Fierer N,van Bodegom PM (2013) Global drivers and patterns of microbial abundance in soil. Global Ecology and Biogeography, 22, 1162-1172. DOI URL
[34]	Sohlenius B (1980) Abundance, biomass and contribution to energy flow by soil nematodes in terrestrial ecosystems. Oikos, 34, 186-194. DOI URL
[35]	Song DG, Pan KW, Tariq A, Sun F, Li ZL, Sun XM, Zhang L, Olusanya OA, Wu XG (2017) Large-scale patterns of distribution and diversity of terrestrial nematodes. Applied Soil Ecology, 114, 161-169. DOI URL
[36]	Song XW, Zhang BC, Bai Y, Pan DF, Deng XD, Wang HS, Sun B, Cao XF (2021) Application and review of biotechnology in promoting protective utilization of black soil. Bulletin of Chinese Academy of Sciences, 36, 1488-1496. (in Chinese with English abstract)
	[ 宋显伟, 张保才, 白洋, 潘多峰, 邓向东, 王竑晟, 孙波, 曹晓风 (2021) 生物技术助力黑土地保护性利用的应用与思考. 中国科学院院刊, 36, 1488-1496.]
[37]	Su LX, Bai TY, Qin XW, Yu H, Wu G, Zhao QY, Tan LH (2021) Organic manure induced soil food web of microbes and nematodes drive soil organic matter under jackfruit planting. Applied Soil Ecology, 166, 103994. DOI URL
[38]	van den Hoogen J, Geisen S, Routh D, Ferris H, Traunspurger W, Wardle DA, de Goede RGM, Adams BJ, Ahmad W, Andriuzzi WS, Bardgett RD, Bonkowski M, Campos-Herrera R, Cares JE, Caruso T, de Brito Caixeta L, Chen XY, Costa SR, Creamer R,Mauro da Cunha Castro J, Dam M, Djigal D, Escuer M, Griffiths BS, Gutiérrez C, Hohberg K, Kalinkina D, Kardol P, Kergunteuil A, Korthals G, Krashevska V, Kudrin AA, Li Q, Liang WJ, Magilton M, Marais M, Martín JAR, Matveeva E, Mayad EH, Mulder C, Mullin P, Neilson R, Nguyen TAD, Nielsen UN, Okada H, Rius JEP, Pan KW, Peneva V, Pellissier L, Carlos Pereira da Silva J, Pitteloud C, Powers TO, Powers K, Quist CW, Rasmann S, Moreno SS, Scheu S, Setälä H, Sushchuk A, Tiunov AV, Trap J, van der Putten WH, Vestergård M, Villenave C, Waeyenberge L, Wall DH, Wilschut R, Wright DG, Yang JI, Crowther TW (2019) Soil nematode abundance and functional group composition at a global scale. Nature, 572, 194-198. DOI URL
[39]	Wilschut RA, Geisen S (2021) Nematodes as drivers of plant performance in natural systems. Trends in Plant Science, 26, 237-247. DOI PMID
[40]	Wilschut RA, Geisen S, Martens H, Kostenko O,de Hollander M, ten Hooven FC, Weser C, Snoek LB, Bloem J, Caković D, Čelik T, Koorem K, Krigas N, Manrubia M, Ramirez K S, Tsiafouli MA, Vreš B, van der Putten WH (2019) Latitudinal variation in soil nematode communities under climate warming-related range-expanding and native plants. Global Change Biology, 5, 2714-2726.
[41]	Wu JH, Chen HL, Zhang YZ (2016) Latitudinal variation in nematode diversity and ecological roles along the Chinese coast. Ecology and Evolution, 6, 8018-8027. DOI PMID
[42]	Xiao HF, Wang WT, Xia SW, Li ZP, Gan JM, Yang XD (2021) Distributional patterns of soil nematodes in relation to environmental variables in forest ecosystems. Soil Ecology Letters, 3, 115-124. DOI
[43]	Xiong D, Wei CZ, Wubs ERJ, Veen GJ, Liang WJ, Wang XB, Li Q, van der Putten WH, Han XG (2020) Nonlinear responses of soil nematode community composition to increasing aridity. Global Ecology and Biogeography, 29, 117-126. DOI
[44]	Yang L, Zhang F, Luo Y, Tang PF (2022) Continuous cotton cropping affects soil micro-food web. Applied Soil Ecology, 171, 104304.
[45]	Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—An outline for soil ecologists. Journal of Nematology, 25, 315-331. PMID
[46]	Zhang GG, Sui X, Li Y, Jia MQ, Wang ZW, Han GD, Wang LC (2020) The response of soil nematode fauna to climate drying and warming in Stipa breviflora desert steppe in Inner Mongolia, China. Journal of Soils and Sediments, 20, 2166-2180. DOI URL
[47]	Zhang SX, Mclaughlin NB, Cui S, Yang XM, Liu P, Wu DH, Liang AZ (2019) Effects of long-term tillage on carbon partitioning of nematode metabolism in a black soil of Northeast China. Applied Soil Ecology, 138, 207-212. DOI URL
[48]	Zhang XY, Sui YY, Zhang XD, Meng K, Herbert SJ (2007) Spatial variability of nutrient properties in black soil of Northeast China. Pedosphere, 17, 19-29. DOI URL