The effects of plant resource inputs on the energy flux of soil nematodes are affected by climate and plant resource type
Lina Zhao, Binbin Yu, Mengmeng Wang, Jie Zhang, Zhifeng Shen, Yang Cui, Junyong Li, Ji Ye, Weizhong Zu, Xiaojing Liu, Zongji Fan, Shenglei Fu, Yuanhu Shao
The effects of plant resource inputs on the energy flux of soil nematodes are affected by climate and plant resource type
• We experimentally reduced litter and root inputs in forests at different latitudes.
• Litter reduction at high and mid latitudes and root removal at low latitudes reduced nematode richness but did not alter nematode abundance.
• The effects of plant resource inputs on nematode energy flux are affected by climate and plant resource type.
The relative abundance of different components of the soil food web can vary tremendously in response to plant resource inputs. However, little is known about the mechanisms that plant resource regulate the energy fluxes and soil community composition. Here, we experimentally reduced litter and root inputs for two years in China at low-, mid-, and high-latitude forests to explore the effects of plant-derived resource inputs on the nematode energy flux and community composition. Litter reduction at high and mid latitudes and root removal at low latitudes reduced nematode richness but did not alter nematode abundance. Besides, Litter reduction reduced energy fluxes of bacterial-feeding nematodes at mid latitudes and energy fluxes of plant-feeding, bacterial-feeding and omnivorous-predatory nematodes at low latitudes, thus reducing the energy fluxes of total nematodes in mid- and low-latitude forests. By contrast, root removal reduced energy fluxes and relative energy flux of plant-feeding nematodes in high- and low-latitude forests. In most cases, nematode diversity in different trophic groups increased with increasing energy flux to nematodes. Taken together, our results suggest that the effects of plant resource inputs on nematode energy flux are affected by climate and plant resource type, which improves our understanding of plant-soil interactions.
Soil nematodes / Leaf litter / Root / Energy flux / Diversity / Trophic groups / Climate / Plant-soil interactions / Soil food web
[1] |
Aho, K., Derryberry, D., Peterson, T., 2014. Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95, 631–636
CrossRef
Google scholar
|
[2] |
Bardgett, R.D., van der Putten, W.H., 2014. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511
CrossRef
Google scholar
|
[3] |
Bardgett, R.D., Wardle, D.A., 2010. Aboveground-belowground linkages. Oxford University Press.
|
[4] |
Bardgett, R.D., Yeates, G.W., Anderson, J.M., 2005. Patterns and Determinants of Soil Biological Diversity. In: Bardgett, R., Usher, M., Hopkins, D., eds. Biological Diversity and Function in Soils. Cambridge University Press, Cambridge, pp. 100–118.
|
[5] |
Barker, K.R., 1985. Nematode extraction and bioassays. An Advanced Treatise on Meloidogyne 2, 19–35.
|
[6] |
Barnes, A.D., Jochum, M., Mumme, S., Haneda, N.F., Farajallah, A., Widarto, T.H., Brose, U., 2014. Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. Nature Communications 5, 5351
CrossRef
Google scholar
|
[7] |
Bongers, T., Ferris, H., 1999. Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology & Evolution 14, 224–228
CrossRef
Google scholar
|
[8] |
Bowden, R.D., Nadelhoffer, K.J., Boone, R.D., Melillo, J., Garrison, J.B., 1993. Contributions of aboveground litter, belowground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest. Canadian Journal of Forest Research 23, 1402–1407
CrossRef
Google scholar
|
[9] |
Butenschoen, O., Scheu, S., Eisenhauer, N., 2011. Interactive effects of warming, soil humidity and plant diversity on litter decomposition and microbial activity. Soil Biology & Biochemistry 43, 1902– 1907
CrossRef
Google scholar
|
[10] |
Chen, D.M., Xing, W., Lan, Z.C., Saleem, M., Wu, Y.Q.Q.G., Hu, S.J., Bai, Y.F., 2018. Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi-arid grassland. Functional Ecology 33, 175–187
CrossRef
Google scholar
|
[11] |
Coleman, D.C., Crossley, D.A. Jr, Hendrix, P.F., 2004. Primary production processes in soils: roots and rhizosphere associates. In: Coleman, D.C., Crossley, D.A., Hendrix, P.F., eds. Fundamentals of Soil Ecology (Second Edition). Academic Press Burlington, pp. 23–46.
|
[12] |
Colloff, M., 2004. Book review: communities and ecosystems: linking the above-ground and below-ground components. Austral Ecology 29, 358–359
CrossRef
Google scholar
|
[13] |
De Ruiter, P.C., Neutel, A.M., Moore, J.C., 1995. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269, 1257–1260
CrossRef
Google scholar
|
[14] |
Ehnes, R.B., Rall, B.C., Brose, U., 2011. Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates. Ecology Letters 14, 993–1000
CrossRef
Google scholar
|
[15] |
Elfstrand, S., Lagerlöf, J., Hedlund, K., Mårtensson, A., 2008. Carbon routes from decomposing plant residues and living roots into soil food webs assessed with 13C labelling. Soil Biology & Biochemistry 40, 2530–2539
CrossRef
Google scholar
|
[16] |
Ferris, H., Bongers, T., 2006. Nematode Indicators of organic enrichment. Journal of Nematology 38, 3–12.
|
[17] |
Freckman, D.W., 1988. Bacterivorous nematodes and organic-matter decomposition. Agriculture, Ecosystems & Environment 24, 195–217
CrossRef
Google scholar
|
[18] |
Ghilarov, M.S., 1977. Why so many species and so many individuals can coexist in the soil. Ecological Bulletins 25, 593–597.
|
[19] |
Gill, R.A., Jackson, R.B., 2000. Global patterns of root turnover for terrestrial ecosystems. New Phytologist 147, 13–31
CrossRef
Google scholar
|
[20] |
Guo, J.X., 1993. Study on litter decomposition in Leymus chinensis grassland-Relation of litter decomposition to ecological environment. Acta Ecologica Sinica, 13, 214–250
|
[21] |
Högberg, P., Nordgren, A., Buchmann, N., Taylor, A.F.S., Ekblad, A., Högberg, M.N., Nyberg, G., Ottosson-Löfvenius, M., Read, D.J., 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792
CrossRef
Google scholar
|
[22] |
Holtkamp, R., Kardol, P., van der Wal, A., Dekker, S.C., van der Putten, W.H., de Ruiter, P.C., 2008. Soil food web structure during ecosystem development after land abandonment. Applied Soil Ecology 39, 23–34
CrossRef
Google scholar
|
[23] |
Hugot, J.P., Baujard, P., Morand, S., 2001. Biodiversity in helminths and nematodes as a field of study: an overview. Nematology 3, 199–208
CrossRef
Google scholar
|
[24] |
Kozdrój, J., van Elsas, J.D., 2000. Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biology & Biochemistry 32, 1405–1417
CrossRef
Google scholar
|
[25] |
Li, J.N., Peng, P.Q., Zhao, J., 2020. Assessment of soil nematode diversity based on different taxonomic levels and functional groups. Soil Ecology Letters 2, 33–39
CrossRef
Google scholar
|
[26] |
Liu, Q., Peng, S.L., Bi, H., Zhang, H.Y., Li, Z.A., Ma, W.H., Li, N.Y., 2006. Nutrient dynamics of foliar litter in reciprocal decomposition in tropical and subtropical forests. Frontiers of Forestry in China 1, 243–252
CrossRef
Google scholar
|
[27] |
Lu, H.B., Liu, S.R., Wang, H., Luan, J.W., Schindlbacher, A., Liu, Y.C., Wang, Y., 2017. Experimental throughfall reduction barely affects soil carbon dynamics in a warm-temperate oak forest, central China. Scientific Reports 7, 15099
CrossRef
Google scholar
|
[28] |
McCann, K., Hastings, A., Huxel, G.R., 1998. Weak trophic interactions and the balance of nature. Nature 395, 794–798
CrossRef
Google scholar
|
[29] |
Meentemeyer, V., 1978. Macroclimate and lignin control of litter decomposition rates. Ecology 59, 465–472
CrossRef
Google scholar
|
[30] |
Moore, J.C., de Ruiter, P.C., Hunt, H.W., Coleman, D.C., Freckman, D.W., 1996. Microcosms and soil ecology: critical linkages between fields studies and modelling food webs. Ecology 77, 694–705
CrossRef
Google scholar
|
[31] |
Nadelhoffer, K.J., Boone, R.D., Bowden, R.D., Canary, J.D., Kaye, J., Micks, P., Ricca, A., Aitkenhead-Peterson, J.A., Lajtha, K., McDowell, W.H., 2004. The DIRT Experiment: litter and Root Influences on Forest Soil Organic Matter Stocks and Function. In: Foster, D., Aber, J., eds. Forest Landscape Dynamics in New England: Ecosystems Structure and Function as a Consequence of 5000 years of Change. Oxford: Oxford University Press.
|
[32] |
Neher, D.A., 2001. Role of nematodes in soil health and their use as indicators. Journal of Nematology 33, 161–168.
|
[33] |
Neher, D.A., 2010. Ecology of plant and free-Living nematodes in natural and agricultural soil. Annual Review of Phytopathology 48, 371–394
CrossRef
Google scholar
|
[34] |
Pausch, J., Hofmann, S., Scharroba, A., Kuzyakov, Y., Ruess, L., 2016. Fluxes of root-derived carbon into the nematode micro-food web of an arable soil. Food Webs 9, 32–38
CrossRef
Google scholar
|
[35] |
Pollierer, M.M., Reinhard, L., Körner, C., Maraun, M., Scheu, S., 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecology Letters 10, 729–736
CrossRef
Google scholar
|
[36] |
Qu, L.R., Wang, C., Bai, E., 2020. Evaluation of the 18O-H2O incubation method for measurement of soil microbial carbon use efficiency. Soil Biology & Biochemistry 145, 107802
CrossRef
Google scholar
|
[37] |
Rooney, N., McCann, K., Gellner, G., Moore, J.C., 2006. Structural asymmetry and the stability of diverse food webs. Nature 442, 265–269
CrossRef
Google scholar
|
[38] |
Rooney, N., McCann, K.S., 2012. Integrating food web diversity, structure and stability. Trends in Ecology & Evolution 27, 40–46
CrossRef
Google scholar
|
[39] |
Scheunemann, N., Maraun, M., Scheu, S., Butenschoen, O., 2015. The role of shoot residues vs. crop species for soil arthropod diversity and abundance of arable systems. Soil Biology & Biochemistry 81, 81–88
CrossRef
Google scholar
|
[40] |
Schwarz, B., Barnes, A.D., Thakur, M.P., Brose, U., Ciobanu, M., Reich, P.B., Rich, R.L., Rosenbaum, B., Stefanski, A., Eisenhauer, N., 2017. Warming alters energetic structure and function but not resilience of soil food webs. Nature Climate Change 7, 895–900
CrossRef
Google scholar
|
[41] |
Shao, Y.H., Wang, X.L., Zhao, J., Wu, J.P., Zhang, W.X., Neher, D.A., Li, Y.X., Lou, Y.P., Fu, S.L., Kardol, P., 2016. Subordinate plants sustain the complexity and stability of soil micro-food webs in natural bamboo forest ecosystems. Journal of Applied Ecology 53, 130–139
CrossRef
Google scholar
|
[42] |
Shao, Y.H., Zhang, W.X., Eisenhauer, N., Liu, T., Ferlian, O., Wang, X.L., Xiong, Y.M., Liang, C.F., Fu, S.L., 2019. Exotic earthworms maintain soil biodiversity by altering bottom-up effects of plants on the composition of soil microbial groups and nematode communities. Biology and Fertility of Soils 55, 213–227
CrossRef
Google scholar
|
[43] |
Soil Survey Staff, 1999. Soil Taxonomy. A Basic System of Soil Classification for Making and Interpreting Soil Surveys. USDA Agriculture Handbook No. 436. U.S. Government Print Office, Washington DC.
|
[44] |
Tardy, V., Mathieu, O., Lévêque, J., Terrat, S., Chabbi, A., Lemanceau, P., Ranjard, L., Maron, P.A., 2014. Stability of soil microbial structure and activity depends on microbial diversity. Environmental Microbiology Reports 6, 173–183
CrossRef
Google scholar
|
[45] |
van den Hoogen, J., Geisen, S., Routh, D., Ferris, H., Traunspurger, W., Wardle, D.A., de Goede, R.G.M., Adams, B.J., Ahmad, W., Andriuzzi, W.S., Bardgett, R.D., Bonkowski, M., Campos-Herrera, R., Cares, J.E., Caruso, T., de Brito Caixeta, L., Chen, X., Costa, S.R., Creamer, R., Mauro da Cunha Castro, J., Dam, M., Djigal, D., Escuer, M., Griffiths, B.S., Gutiérrez, C., Hohberg, K., Kalinkina, D., Kardol, P., Kergunteuil, A., Korthals, G., Krashevska, V., Kudrin, A.A., Li, Q., Liang, W., Magilton, M., Marais, M., Martín, J.A.R., Matveeva, E., Mayad, E.H., Mulder, C., Mullin, P., Neilson, R., Nguyen, T.A.D., Nielsen, U.N., Okada, H., Rius, J.E.P., Pan, K., Peneva, V., Pellissier, L., Carlos Pereira da Silva, J., Pitteloud, C., Powers, T.O., Powers, K., Quist, C.W., Rasmann, S., Moreno, S.S., Scheu, S., Setälä, H., Sushchuk, A., Tiunov, A.V., Trap, J., van der Putten, W., Vestergård, M., Villenave, C., Waeyenberge, L., Wall, D.H., Wilschut, R., Wright, D.G., Yang, J.I., Crowther, T.W., 2019. Soil nematode abundance and functional group composition at a global scale. Nature 572, 194–198
CrossRef
Google scholar
|
[46] |
Wardle, D.A., 2005. How Plant Communities Influence Decomposer Communities. In: Bardgett, R.D., Usher, M.B., Hopkins, D.W., eds. Biological Diversity and Function in Soils. Cambridge University Press Cambridge, pp. 119–138.
|
[47] |
Wardle, D.A., 2006. The influence of biotic interactions on soil biodiversity. Ecology Letters 9, 870–886
CrossRef
Google scholar
|
[48] |
Wardle, D.A., 2010. Communities and ecosystems: Linking the above-ground and below-ground components. Austral Ecology 29, 358–359.
|
[49] |
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633
CrossRef
Google scholar
|
[50] |
Wilschut, R.A., Geisen, S., 2020. Nematodes as drivers of plant performance in natural systems. Trends in Plant Science, 26, 239–247
CrossRef
Google scholar
|
[51] |
Yeates, G.W., 1979. Soil nematodes in terrestrial ecosystems. Journal of Nematology 11, 213–229.
|
[52] |
Yeates, G.W., Bongers, T., 1999. Nematode diversity in agroecosystems. Agriculture, Ecosystems & Environment 74, 113–135
CrossRef
Google scholar
|
[53] |
Yeates, G.W., Bongers, T., De Goede, R.G.M., Freckman, D.W., Georgieva, S.S., 1993. Feeding habits in soil nematode families and genera-an outline for soil ecologists. Journal of Nematology 25, 315–331.
|
[54] |
Yu, S.Q., Chen, Y.Q., Zhao, J., Fu, S.L., Li, Z.A., Xia, H.P., Zhou, L.X., 2017. Temperature sensitivity of total soil respiration and its heterotrophic and autotrophic components in six vegetation types of subtropical China. Science of the Total Environment 607–608, 160–167
CrossRef
Google scholar
|
[55] |
Zhang, Q., 2011. Dinghushan National Field Research Station of Forest Ecosystem (1998-2008). In: Sun, H.L., Yu, G.R., Ouyang, Z., He, H.L., eds. Chinese Ecosystem Research Network Dataset. Forest Ecosystems.
|
[56] |
Zhao, J., Xiao, J., Zhang, W., Fu, Z.Y., Zhang, M.Y., Liu, T., Tan, Q.J., Wang, K.L., 2019. A method for estimating nematode body lengths for use in the calculation of biomass via a simplified formula. Soil Biology & Biochemistry 134, 36–41
CrossRef
Google scholar
|
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