Abstract
Healthy soils are of pivotal importance in sustainable production of fruits and vegetables, as majority of soil functions rely on the diversity and complexity of soil food webs. A five-month field experiment was conducted under an organic strawberry production system to better understand soil food web dynamics indicated by changes in soil nematode communities after two commonly used mulch treatments (grass hay and black geotextile). In addition to the traditional methods (diversity and community indices) in nematode ecology, we applied network analysis to identify the key relationships between nematode taxa/feeding groups under different mulching systems. Soil nematodes were significantly influenced by sampling time and mulch treatments during the study period. Total density of nematodes was lower in both non-mulched and covered soils compared to pre-plant levels. Effective species number (Hill’s number) of soil nematodes was higher in plots covered with geotextile as a result of the treatment. Significant difference was observed in community composition among treatments and sampling times. Although bacterial feeders dominated in almost all samples, relative abundance of fungivores increased by the end of summer. Organic mulched soils had the highest proportion of herbivores, significantly differing from untreated plots. Soil food web analysis showed that nematode assemblages became less structured and more degraded in all soils compared to the initial conditions. However, mulch applications enhance functional diversity and connectivity of assemblages, regardless of mulch type. These changes suggest a more stable soil ecosystem with higher functional resilience and adaptive capacity which is crucial to ensure viability and sustainability of agricultural production.
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REFERENCES
M. M. M. Abd-Elgawad, “Plant-parasitic nematodes of strawberry in Egypt: a review,” Bull. Natl. Res. Cent. 43 (1), 7 (2019). https://doi.org/10.1186/s42269-019-0049-2
H. J. Atkinson, “Respiration in nematodes,” in Nematodes as Biological Models, Vol. 2: Aging and Other Model Systems, Ed. by B. M. Zuckerman (Academic, New York, 1980), pp. 101–142.
G. Baermann, “Eine einfache Methode zur Auffindung von Ankylostomum-(Nematoden)-Larven In Erdproben,” Geneeskd. Tijdschr. Ned.-Indie 57, 131–137 (1917).
G. Bakonyi, P. Nagy, E. Kovács-Láng, E. Kovács, S. Barabás, V. Répási, and A. Seres, “Soil nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland,” Appl. Soil Ecol. 37 (1–2), 31–40 (2007). https://doi.org/10.1016/j.apsoil.2007.03.008
R. D. Bardgett and D. A. Wardle, Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change (Oxford University Press, Oxford, 2010).
E. Barrios, “Soil biota, ecosystem services and land productivity,” Ecol. Econ. 64 (2), 269–285 (2007). https://doi.org/10.1016/j.ecolecon.2007.03.004
R. Berkelmans, H. Ferris, M. Tenuta, and A. H. C. van Bruggen, “Effects of long-term crop management on nematode trophic levels other than plant feeders disappear after 1 year of disruptive soil management,” Appl. Soil Ecol. 23 (3), 223–235 (2003). https://doi.org/10.1016/S0929-1393(03)00047-7
T. Bongers, De Nematoden van Nederland (Wageningen Agricultural University, Wageningen, 1989) [in Dutch].
T. Bongers, “The maturity index: an ecological measure of environmental disturbance based on nematode species composition,” Oecologia 83 (1), 14–19 (1990). https://doi.org/10.1007/BF00324627
T. Bongers and M. Bongers, “Functional diversity of nematodes,” Appl. Soil Ecol. 10 (3), 239–251 (1998). https://doi.org/10.1016/S0929-1393(98)00123-1
T. Bongers and H. Ferris, “Nematode community structure as a bioindicator in environmental monitoring,” Trends Ecol. Evol. 14 (6), 224–228 (1999). https://doi.org/10.1016/S0169-5347(98)01583-3
L. R. Bulluck, K. R. Barker, and J. B. Ristaino, “Influences of organic and synthetic soil fertility amendments on nematode trophic groups and community dynamics under tomatoes,” Appl. Soil Ecol. 21 (3), 233–250 (2002). https://doi.org/10.1016/S0929-1393(02)00089-6
D. Chen, S. Zheng, Y. Shan, F. Taube, and Y. Bai, “Vertebrate herbivore-induced changes in plants and soils: Linkages to ecosystem functioning in a semi-arid steppe,” Funct. Ecol. 27 (1), 273–281 (2013). https://doi.org/10.1111/1365-2435.12027
V. Cochran, S. Sparrow, and E. Sparrow, “Residue effects on soil micro- and macroorganisms,” in Managing Agricultural Residues, Ed. by P. W. Unger (CRC Press, Boca Raton, FL, 1994), pp. 163–184.
V. Coudrain, M. Hedde, M. Chauvat, P.-A. Maron, E. Bourgeois, B. Mary, et al., “Temporal differentiation of soil communities in response to arable crop management strategies,” Agric. Ecosyst. Environ. 225, 12–21 (2016). https://doi.org/10.1016/j.agee.2016.03.029
R. E. Creamer, S. E. Hannula, J. P. V. Leeuwen, D. Stone, M. Rutgers, R. M. Schmelz, et al., “Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe,” Appl. Soil Ecol. 97, 112–124 (2016). https://doi.org/10.1016/j.apsoil.2015.08.006
G. Csárdi and T. Nepusz, “The igraph software package for complex network research,” Int. J. Complex Syst. 1695 (5), 1–9 (2006).
D. Djigal, S. Saj, B. Rabary, E. Blanchart, and C. Villenave, “Mulch type affects soil biological functioning and crop yield of conservation agriculture systems in a long-term experiment in Madagascar,” Soil Tillage Res. 118, 11–21 (2012). https://doi.org/10.1016/j.still.2011.10.008
J. W. Doran, “Soil health and global sustainability: Translating science into practice,” Agric. Ecosyst. Environ. 88 (2), 119–127 (2002). https://doi.org/10.1016/S0167-8809(01)00246-8
S. T. DuPont, H. Ferris, and M. van Horn, “Effects of cover crop quality and quantity on nematode-based soil food webs and nutrient cycling,” Appl. Soil Ecol. 41 (2), 157–167 (2009). https://doi.org/10.1016/j.apsoil.2008.10.004
European Food Safety Authority, “Opinion of the Scientific Panel on Plant protection products and their residues (PPR) related to the revision of Annexes II and III to Council Directive 91/414/EEC concerning the placing of plant protection products on the market-Ecotoxicological studies,” EFSA J. 5 (3), 461 (2007). https://doi.org/10.2903/j.efsa.2007.461
H. Ferris, T. Bongers, and R. G. M. de Goede, “A framework for soil food web diagnostics: Extension of the nematode faunal analysis concept,” Appl. Soil Ecol. 18 (1), 13–29 (2001). https://doi.org/10.1016/S0929-1393(01)00152-4
H. Ferris, S. Sánchez-Moreno, and E. B. Brennan, “Structure, functions and interguild relationships of the soil nematode assemblage in organic vegetable production,” Appl. Soil Ecol. 61, 16–25 (2012). https://doi.org/10.1016/j.apsoil.2012.04.006
D. A. Fiscus and D. A. Neher, “Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances,” Ecol. Appl. 12 (2), 565–575 (2002). https://doi.org/10.1890/1051-0761(2002)012[0565:DSOFLS]2.0.CO;2
T. A. Forge, E. Hogue, G. Neilsen, and D. Neilsen, “Effects of organic mulches on soil microfauna in the root zone of apple: implications for nutrient fluxes and functional diversity of the soil food web,” Appl. Soil Ecol. 22 (1), 39–54 (2003). https://doi.org/10.1016/S0929-1393(02)00111-7
T. A. Forge, E. J. Hogue, G. Neilsen, D. Neilsen, “Organic mulches alter nematode communities, root growth and fluxes of phosphorus in the root zone of apple,” Appl. Soil Ecol. 39 (1), 15–22 (2008). https://doi.org/10.1016/j.apsoil.2007.11.004
D. M. Griffin, “Water potential as a selective factor in the microbial ecology of soils”, in Water Potential Relations in Soil Microbiology, Ed. by J. F. Parr, W. R. Gardner, and L. F. Elliott (Soil Science Society of America, Madison, WI, 1981), pp. 141–151. https://doi.org/10.2136/sssaspecpub9.c5
B. S. Griffiths, A. G. Bengough, R. Neilson, and D. L. Trudgill, “The extent to which nematode communities are affected by soil factors—a pot experiment,” Nematology 4 (8), 943–952 (2002). https://doi.org/10.1163/156854102321122566
B. S. Griffiths, R. Neilson, and A. G. Bengough, “Soil factors determined nematode community composition in a two year pot experiment,” Nematology 5 (6), 889–897 (2003). https://doi.org/10.1163/156854103773040808
M. O. Hill, “Diversity and evenness: a unifying notation and its consequences,” Ecology 54 (2), 427–432 (1973). https://doi.org/10.2307/1934352
Cultivation and use of major fruits (2014–), Hungarian Central Statistical Office. https://www.ksh.hu/docs/ hun/xstadat/xstadat_eves/i_omn006l.html. Accessed February 23, 2021.
Main data of meteorological observation stations (1985–), Hungarian Central Statistical Office. https://ksh.hu/docs/hun/xstadat/xstadat_eves/xls/5_ 10_4i.xls?lang=hu. Accessed February 23, 2021.
M. D. Hunter and P. W. Price, “Playing chutes and ladders: Heterogeneity and the relative roles of bottom-up and top-down forces in natural communities,” Ecology 73 (3), 724–732 (1992).
IUSS Working Group WRB, World Reference Base for Soil Resources 2014, Update 2015, International Soil Classification System for Naming Soils and Creating Legends for Soil Maps, World Soil Resources Reports No. 106 (UN Food and Agriculture Organization, Rome, 2015).
K. Jabran, Role of Mulching in Pest Management and Agricultural Sustainability (Springer-Verlag, Cham, 2019)
E. Laliberté and P. Legendre, “A distance-based framework for measuring functional diversity from multiple traits,” Ecology 91 (1), 299–305 (2010). https://doi.org/10.1890/08-2244.1
E. Laliberté, P. Legendre, and B. Shipley, FD: measuring functional diversity from multiple traits, and other tools for functional ecology, Version 1.0-12, 2014. https://cran.r-project.org/web/packages/FD/FD.pdf. Accessed February 23, 2021.
R. V. Lenth, “Least-squares means: the R package lsmeans,” J. Stat. Soft. 69 (1), 1–33 (2016). https://doi.org/10.18637/jss.v069.i01
T. Liu, X. Chen, F. Hu, W. Ran, Q. Shen, H. Li, and J. K. Whalen, “Carbon-rich organic fertilizers to increase soil biodiversity: evidence from a meta-analysis of nematode communities,” Agric. Ecosyst. Environ. 232, 199–207 (2016). https://doi.org/10.1016/j.agee.2016.07.015
R. McSorley, K.-H. Wang, and G. Church, “Suppression of root-knot nematodes in natural and agricultural soils,” Appl. Soil Ecol. 39 (3), 291–298 (2008). https://doi.org/10.1016/j.apsoil.2008.01.002
M. M. Mezeli, S. Page, T. S. George, R. Neilson, A. Mead, M. S. A. Blackwell, and P. M. Haygarth, “Using a meta-analysis approach to understand complexity in soil biodiversity and phosphorus acquisition in plants,” Soil Biol. Biochem. 142, 107695 (2020). https://doi.org/10.1016/j.soilbio.2019.107695
J. Michalski and Z. Cheng, “Effects of “lights out” turfgrass renovation on plants, soil arthropod and nematode communities,” Appl. Soil Ecol. 127, 144–154 (2018). https://doi.org/10.1016/j.apsoil.2018.03.016
M.-T. Mueller, H. Fueser, S. Höss, and W. Traunspurger, “Species-specific effects of long-term microplastic exposure on the population growth of nematodes, with a focus on microplastic ingestion,” Ecol. Indic. 118, 106698 (2020). https://doi.org/10.1016/j.ecolind.2020.106698
M. S. Nahar, P. S. Grewal, S. A. Miller, D. Stinner, B. R. Stinner, M. D. Kleinhenz, et al., “Differential effects of raw and composted manure on nematode community, and its indicative value for soil microbial, physical and chemical properties,” Appl. Soil Ecol. 34 (2–3), 140–151 (2006). https://doi.org/10.1016/j.apsoil.2006.03.011
D. A. Neher, “Role of nematodes in soil health and their use as indicators,” J. Nematol. 33 (4), 161–168 (2001).
Y. Oka, “Mechanisms of nematode suppression by organic soil amendments—A review,” Appl. Soil Ecol. 44 (2), 101–115 (2010). https://doi.org/10.1016/j.apsoil.2009.11.003
J. Oksanen, F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, et al., “vegan: Community ecology package, Version 2.5-6, 2019. https://CRAN. R-project.org/package=vegan. Accessed February 23, 2021.
F. Pan, N. Li, W. Zou, X. Han, and N. B. McLaughlin, “Soil nematode community structure and metabolic footprint in the early pedogenesis of a mollisol,” Eur. J. Soil Biol. 77, 17–25 (2016). https://doi.org/10.1016/j.ejsobi.2016.09.004
J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, and R Core Team, nlme: Linear and nonlinear mixed effects models, Version 3.1-142, 2019. https://CRAN.R-project.org/ package=nlme. Accessed February 23, 2021.
D. L. Porazinska, L. W. Duncan, R. McSorley, and J. H. Graham, “Nematode communities as indicators of status and processes of a soil ecosystem influenced by agricultural management practices,” Appl. Soil Ecol. 13 (1), 69–86 (1999). https://doi.org/10.1016/S0929-1393(99)00018-9
L. Rahman, K. Y. Chan, and D. P. Heenan, “Impact of tillage, stubble management and crop rotation on nematode populations in a long-term field experiment,” Soil Tillage Res. 95 (1–2), 110–119 (2007). https://doi.org/10.1016/j.still.2006.11.008
R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2015). http://www. R‑project.org. Accessed February 23, 2021.
K. Ritz and D. L. Trudgill, “Utility of nematode community analysis as an integrated measure of the functional state of soils: perspectives and challenges,” Plant Soil 212, 1–11 (1999). https://doi.org/10.1023/A:1004673027625
H. Y. Samaliev and M. Mohamedova, “Plant-parasitic nematodes associated with strawberry (Fragaria aiianassa Duch.) in Bulgaria,” Bulg. J. Agric. Sci. 17 (6), 730–735 (2011).
S. Sánchez-Moreno, L. Jiménez, J. L. Alonso-Prados, and J. M. García-Baudín, “Nematodes as indicators of fumigant effects on soil food webs in strawberry crops in Southern Spain,” Ecol. Indic. 10 (2), 148–156 (2010). https://doi.org/10.1016/j.ecolind.2009.04.010
B. Sieriebriennikov, H. Ferris, and R. G. M. de Goede, “NINJA: an automated calculation system for nematode-based biological monitoring,” Eur. J. Soil Biol. 61, 90–93 (2014). https://doi.org/10.1016/j.ejsobi.2014.02.004
R. A. Sikora and E. Fernández, “Nematode parasites of vegetables”, in Plant Parasitic Nematodes in Subtropical and Tropical Agriculture, Ed. by M. Luc, R. A. Sikora, and J. Bridge, 2nd ed. (CAB International, Wallingford, 2005), pp. 319–392.
Z. Steinmetz, C. Wollmann, M. Schaefer, C. Buchmann, J. David, J. Tröger, et al., “Plastic mulching in agriculture. Trading short-term agronomic benefits for long-term soil degradation?” Sci. Total Environ. 550, 690–705 (2016). https://doi.org/10.1016/j.scitotenv.2016.01.153
G. R. Stirling and L. M. Eden, “The impact of organic amendments, mulching and tillage on plant nutrition, Pythium root rot, root-knot nematode and other pests and diseases of capsicum in a subtropical environment, and implications for the development of more sustainable vegetable farming systems,” Austr. Plant Pathol. 37 (2), 123–131 (2008). https://doi.org/10.1071/AP07090
T. Thoden, G. Korthals, and A. Termorshuizen, “Organic amendments and their influences on plant-parasitic and free-living nematodes: A promising method for nematode management?” Nematology 13 (2), 133–153 (2011). https://doi.org/10.1163/138855410X541834
K.-H. Wang and R. McSorley, Effects of soil ecosystem management on nematode pests, nutrient cycling, and plant health, APSnet Features, 2005. https:// www.apsnet.org/edcenter/apsnetfeatures/Pages/SoilEcosystemManagement.aspx. Accessed February 23, 2021)
K.-H. Wang, R. McSorley, and N. Kokalis-Burelle, “Effects of cover cropping, solarization, and soil fumigation on nematode communities,” Plant Soil 286 (1–2), 229–243 (2006). https://doi.org/10.1007/s11104-006-9040-4
K.-H. Wang, N. Kokalis-Burelle, R. McSorley, and R. Gallaher, “Cover crops and organic mulches for nematode, weed and plant health management,” Nematology 10 (2), 231–242 (2008). https://doi.org/10.1163/156854108783476412
D. A. Wardle, G. W. Yeates, R. N. Watson, and K. S. Nicholson, “The detritus food-web and the diversity of soil fauna as indicators of disturbance regimes in agro-ecosystems,” Plant Soil 170 (1), 35–43 (1995). https://doi.org/10.1007/BF02183053
D. J. Watts and S. H. Strogatz, “Collective dynamics of ‘small-world’ networks,” Nature 393, 440–442 (1998). https://doi.org/10.1038/30918
H. Wickham, ggplot2: Elegant Graphics for Data Analysis, 2nd ed. (Springer, Cham, 2016)
G. W. Yeates, “Variation of pasture nematode populations over thirty-six months in a summer dry silt loam,” Pedobiologia 24, 329–346 (1982).
G. W. Yeates, T. Bongers, R. G. de Goede, D. W. Freckman, and S. S. Georgieva, “Feeding habits in soil nematode families and genera-an outline for soil ecologists,” J. Nematol. 25 (3), 315–331 (1993).
G. W. Yeates, D. A. Wardle, and R. N. Watson, “Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period,” Soil Biol. Biochem. 31 (12), 1721–1733 (1999). https://doi.org/10.1016/S0038-0717(99)00091-7
G. W. Yeates, “Diversity of nematodes,” in Biodiversity in Agricultural Production Systems, Ed. by G. Benckiser and S. Schnell (CRC Press, Boca Raton, FL, 2007), pp. 215–235.
I. Zasada, C. Rice, and S. Meyer, “Improving the use of rye (Secale cereale) for nematode management: potential to select cultivars based on Meloidogyne incognita host status and benzoxazinoid content,” Nematology 9 (1), 53–60 (2007). https://doi.org/10.1163/156854107779969745
S. Zhong, H. Zeng, and Z. Jin, “Influences of different tillage and residue management systems on soil nematode community composition and diversity in the tropics,” Soil Biol. Biochem. 107, 234–243 (2017). https://doi.org/10.1016/j.soilbio.2017.01.007
ACKNOWLEDGMENTS
We are grateful to Dr. Péter Nagy (Szent István University) for nematode identification, and Ágnes Vajda (University of Veterinary Medicine Budapest) for her help in field works. We thank the garden crew and the students of the John von Neumann University for their assistance with mulching, crop planting, irrigation, and harvesting operations.
Funding
This research was funded by the European Union and co-financed by the European Social Fund [grant agreement no. EFOP-3.6.2-16-2017-00012, project title: Development of a product chain model for functional, healthy and safe foods from farm to fork based on a thematic research network].
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Tóth, Z., Király, I., Mihálka, V. et al. Changes in Composition and Connectivity of Soil Nematode Assemblages under Different Mulching Systems in a Strawberry Field Experiment. Eurasian Soil Sc. 54, 1705–1720 (2021). https://doi.org/10.1134/S1064229321110132
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DOI: https://doi.org/10.1134/S1064229321110132