Caracterización de la comunidad de nematodos de suelo encuatro sistemas productivos del sudeste bonaerense, Argentina

Andrea J. Thougnon Islas; Eliseo Chaves; Dora Carmona; Silvina San Martino; Eduardo Mondino

doi:10.25260/EA.24.34.2.0.2237

Authors

Andrea J. Thougnon Islas Instituto de Innovación para la Producción Agropecuaria y el Desarrollo Sostenible (IPADS Balcarce). Estación Experimental Agropecuaria INTA Balcarce-CONICET, Argentina. Unidad Integrada Balcarce, Estación Experimental Agropecuaria INTA Balcarce-Facultad de Ciencias Agrarias Universidad Nacional de Mar del Plata, Argentina
Eliseo Chaves Nema-Agris, La Plata, Argentina
Dora Carmona Unidad Integrada Balcarce, Estación Experimental Agropecuaria INTA Balcarce-Facultad de Ciencias Agrarias Universidad Nacional de Mar del Plata, Argentina
Silvina San Martino Unidad Integrada Balcarce, Estación Experimental Agropecuaria INTA Balcarce-Facultad de Ciencias Agrarias Universidad Nacional de Mar del Plata, Argentina
Eduardo Mondino Unidad Integrada Balcarce, Estación Experimental Agropecuaria INTA Balcarce-Facultad de Ciencias Agrarias Universidad Nacional de Mar del Plata, Argentina

DOI:

https://doi.org/10.25260/EA.24.34.2.0.2237

Keywords:

soil nematodes, trophic groups, nematode assemblage, soil health

Abstract

This work evaluates the community of soil nematodes in agricultural and livestock environments with different intensity of land use in the southeast of the province of Buenos Aires. Nematodes were extracted from sites with different intensity of land use: corn (2 consecutive years of conventional tillage [LC]), potato (1 year of LC), soybean (direct seeding), and pastures (with grazing animals). 44 genera of nematodes belonging to 5 trophic groups were identified. The most abundant genera were Helicotylenchus, Pratylenchus and Cruznema. Significant differences were found in the structure of the nematode community between land uses. The total abundance and by trophic groups was higher in soybeans and pasture. Furthermore, in relation to the composition of the community of free-living nematodes (bacteriophages, frugivores, omnivores and predators), the sites with corn and soybeans presented a higher proportion of fungivores, while the sites with potatoes and grass showed a higher proportion of bacteriophages. In relation to phytophagous nematodes, the community associated with sites with greater agricultural disturbance (corn and potatoes) presented a different and less diverse assembly than those associated with sites with less disturbance (soybean and pasture). The nematological indices showed that the successional dynamics of the nematode communities were affected due to land use practices. This was confirmed through the analysis of the faunal profile, the majority of food chains, regardless of the type of land use, were affected by agronomic practices showing mature food webs. This work constitutes the first report on the composition of soil nematode communities in agricultural and livestock production fields in southeastern Buenos Aires, and contributes to understanding the ecology of soil nematode communities impacted by different anthropogenic practices.

References

Aitchison, J. 1982. The statistical analysis of compositional data. Journal of the Royal Statistical Society, Series B (Methodological) 44(2):139-160. https://doi.org/10.1111/j.2517-6161.1982.tb01195.x.

Aitchison, J. 2005. A concise guide to compositional data analysis. 2do Compos Data Anal Workshop CoDaWork 5:17-21.

Biswal, D. 2022. Nematodes as ghosts of land use past: elucidating the roles of soil nematode community studies as indicators of soil health and land management practices. Applied Biochemistry and Biotechnology 194(5):2357-2417. https://doi.org/10.1007/s12010-022-03808-9.

Bongers, T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83(1):14-19. https://doi.org/10.1007/BF00324627.

Bongers, T., H. van der Meulen, and G. Korthals. 1997. Inverse relationship between the nematode maturity index and plant parasite index under enriched nutrient conditions. Applied Soil Ecology 6(2):1995-199. https://doi.org/10.1016/S0929-1393(96)00136-9.

Bongers, T. 1999. The maturity index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. Plant and Soil 212(1):13-22. https://doi.org/10.1023/A:1004571900425.

Bongers, T., and M. Bongers. 1998. Functional diversity of nematodes. Applied Soil Ecology 10(3):239-251. https://doi.org/10.1016/S0929-1393(98)00123-1.

Borcard, D., F. Gillet, and P. Legendre. 2011. Numerical ecology with R. Springer, New York, USA. https://doi.org/10.1007/978-3-319-71404-2.

Bray, R. H., and L. Kurtz. 1945. Determination of total, organic, and available forms of phosphorus in soils. Soil Science 59(1):39-46. https://doi.org/10.1097/00010694-194501000-00006.

Bonkowski, M., C. Villenave, and B. Griths. 2009. Rhizosphere fauna: The functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 321:213-233. https://doi.org/10.1007/s11104-009-0013-2.

Bünemann, E. K., G. Bongiorno, Z. Bai, R. E. Creamer, G. De Deyn, et al. 2018. Soil quality-A critical review. Soil Biology and Biochemistry 120:105-125. https://doi.org/10.1016/j.soilbio.2018.01.030.

Chaves, E. J., G. Cap, M. Torres, and M. M. Echeverría. 1998. Informe del plan de trabajo Caracterización y distribución de nematodos de importancia cuarentenaria en la provincia de Buenos Aires. INTA. Programa 13-0173. EEA Balcarce. Pp. 19.

Chaves, E. J., and M. Torres. 1993. Nematodes parásitos de la papa del sudeste bonaerense. Boletín Técnico Nº 115. Pp. 21.

Chaves, E. J., M. M. Echeverria, H. Merlo Álvarez, and A. Salas. 2019. Clave para determinar géneros de nematodos del suelo de la República Argentina. Fundación de Historia Natural Félix de Azara Centro de Ciencias Naturales y Antropológicas Universidad Maimónides, Buenos Aires.

De Cáceres, M., F. Jansen, and N. Dell. 2016. Indicspecies: relationship between species and groups of sites. R package version 1(6).

De Cáceres, M., and P. Legendre. 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90(12):3566-74. https://doi.org/10.1890/08-1823.1.

Dean, A., D. Voss, and D. Draguljić. 2017. Design and analysis of experiments, 2nd edition, Springer, New York. https://doi.org/10.1007/978-3-319-52250-0.

Demétrio, C. G. B., J. Hinde, and R. A. Moral. 2014. Models for overdispersed data in entomology. Pp. 219-259 en C. P. Ferreira and W. A. C. Godoy (eds.). Ecological Modelling Applied to Entomology. Entomology in Focus. Vol 1. Springer, Cham. https://doi.org/10.1007/978-3-319-06877-0_9.

Dietrich, P., A. Roeder, S. Cesarz, N. Eisenhauer, A. Ebeling, et al. 2020. Nematode communities, plant nutrient economy and life‐cycle characteristics jointly determine plant monoculture performance over 12 years. Oikos 129(4) 466-479. https://doi.org/10.1111/oik.06989.

Dunn, P. K., and G. K. Smith. 2018. Generalized linear models with examples in R. Springer, New York. https://doi.org/10.1007/978-1-4419-0118-7.

Du Preez, G., M. Daneel, R. De Goede, M. J. Du Toit, H. Ferris, et al. 2022. Nematode-based indices in soil ecology: Application, utility, and future directions. Soil Biology and Biochemistry 169:108640. https://doi.org/10.1016/j.soilbio.2022.108640.

Ferris, H., T. Bongers, and R. De Goede. 2001. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 18(1):13-29. https://doi.org/10.1016/S0929-1393(01)00152-4.

Fiscus, D. A., and D. A. Neher. 2002. Distinguishing sensitivity of free‐living soil nematode genera to physical and chemical disturbances. Ecological Applications 12(2):565-575. https://doi.org/10.2307/3060963.

Frampton, G. K. 1997. The potential of Collembola as indicators of pesticide usage: evidence and methods from the UK arable ecosystem. Pedobiologia 41(1):179-184. https://doi.org/10.1016/S0031-4056(24)02992-5.

Galecki, A., and T. Burzykowski. 2013. Linear mixed-effects models using R. Springer, New York. https://doi.org/10.1007/978-1-4614-3900-4.

Haynes, R., R. Swift, and R. Stephen. 1991. Influence of mixed cropping rotations (pasture-arable) on organic matter content, water stable aggregation and clod porosity in a group of soils. Soil and Tillage Research 19(1):77-87. https://doi.org/10.1016/0167-1987(91)90111-A.

Helgason, B. L., F. L. Walley, and J. J. Germida. 2009. Fungal and bacterial abundance in long-term no-till and intensive-till soils of the Northern Great Plains. Soil Science Society of America Journal 73(1):120-127. https://doi.org/10.2136/sssaj2007.0392.

Heyns, J. 1971. A guide to the plant and soil nematodes of South Africa. Balkema, AA. Cape Town. Pp. 233.

Carneiro de Lima da Silva, J. V., M. N. C. Hirschfeld, J. E. Cares, and A. M. Esteves. 2020. Land use, soil properties and climate variables influence the nematode communities in the Caatinga dry forest. Applied Soil Ecology 150:103474. https://doi.org/10.1016/j.apsoil.2019.103474.

Hooper, D. 1986. Handling, fixing, staining, and mounting nematodes. Pp. 50-58 en J. Southey (ed.). Laboratory methods for work with plant and soil nematodes. Reference Book 402. Ministry of Agriculture, London, UK.

Hydbom, S., M. Ernfors, J. Birgander, J. Hollander, E. S. Jensen, et al. 2017. Reduced tillage stimulated symbiotic fungi and microbial saprotrophs but did not lead to a shift in the saprotrophic microorganism community structure. Applied Soil Ecology 119:104-114. https://doi.org/10.1016/j.apsoil.2017.05.032.

Ingham, R. E., J. A. Trofymow, E. R. Ingham, and D. C. Coleman. 1985. Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55(1):119-140. https://doi.org/10.2307/1942528.

Ito, T., M. Araki, M. Komatsuzaki, N. Kaneko, and H. Ohta. 2015. Soil nematode community structure affected by tillage systems and cover crop managements in organic soybean production. Appl Soil Ecol 86:137-147. https://doi.org/10.1016/j.apsoil.2014.10.003.

Jenkins, W. 1964. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Ddisease Reporter 48(9):692.

Khan, Z., and Y. H. Kim. 2007. A review on the role of predatory soil nematodes in the biological control of plant parasitic nematodes. Applied Soil Ecology 35(2):370-379. https://doi.org/10.1016/j.apsoil.2006.07.007.

Kassambara, A., and F. Mundt. 2020. factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R package version 1.0.7.

Keeney, D. R. 1982. Nitrogen-availability indices. Pp. 711-733 en A. L. Page (ed.). Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy. Soil Science Society of America. Madison, WI. https://doi.org/10.2134/agronmonogr9.2.2ed.c33.

Keeney, D. R., and D. W. Nelson. 1982. Nitrogen inorganic forms. Pp. 643-698 en A. L. Page (ed.). Methods of soil analysis. Part 2. Chemical and microbiological properties. 2da edición. American Society of Agronomy. Soil Science Society of America. Madison, Wiscosin, USA. https://doi.org/10.2134/agronmonogr9.2.2ed.c33.

Kimenju, J., N. Karanja, G. K. Mutua, B. Rimberia, and P. Wachira. 2009. Nematode community structure as influenced by land use and intensity of cultivation. Tropical and Subtropical Agroecosystems 11(2):353-360.

Le, S., J. Josse, and F. Husson. 2008. FactoMineR: An R Package for Multivariate Analysis. Journal of Statistical Software 25(1):1-18. https://doi.org/10.18637/jss.v025.i01.

Leco. 2013. Organic application notes. URL: leco.com.

Lehmann, J., D. A. Bossio, I. Kögel-Knabner, and M. C. Rillig. 2020. The concept and future prospects of soil health. Nature Reviews Earth and Environment 1:544-553. https://doi.org/10.1038/s43017-020-0080-8.

Lenth, R. V. 2021. emmeans: Estimated Marginal Means, akaLeast-Squares Means. R package version 1.6.3.

Li, Y., G. Yang, D. A. Neher, C. Y. Xu, and J. Wu. 2015. Status of soil nematode communities during natural regeneration of a subtropical forest in southwestern China. Nematology 17:79-90. https://doi.org/10.1163/15685411-00002853.

Lu, Q., T. Liu, N. Wang, Z. Dou, K. Wang, et al. 2020. A review of soil nematodes as biological indicators for the assessment of soil health. Front Agric Sci Eng 7:275-281. https://doi.org/10.15302/J-FASE-2020327.

Mc-Cullagh, P., and J. Nelder. 1989. Generalized linear models. Chapman and Hall, London. https://doi.org/10.1007/978-1-4899-3242-6.

Marais, M., A. Swart, H. Fourie, S. D. Berry, R. Knoetze, et al. 2017. Techniques and procedures. Pp. 73-118 en H. Fourie, V. W. Spaull, R. K. Jones, M. S. Daneel and D. De Waele (eds.). Nematology in South Africa: a View from the 21st Century. Springer, Cham. https://doi.org/10.1007/978-3-319-44210-5_4.

Mondino, E. A. 2010. Comunidade de nematoides do solo, no ecossistema do Pampa Austral da Argentina, sob diferentes sistemas de cultivo. Tesis doctoral. Universidade Federal Rural do Rio de Janeiro. Pp. 102.

Mondino, E. A., E. J. Chaves, and G. A. Studdert. 2001. Efecto de las rotaciones, las labranzas y la fertilización nitrogenada sobre la nematofauna del suelo. Tesis de Maestría en Producción Vegetal. Facultad de Ciencias Agrarias. Pp. 66.

Moral, R. A., J. Hinde, and C. G. B. Demétrio. 2017. Half-normal plots and overdispersed models in R: the hnp package. Journal of Statistical Software 81(10):1-23. https://doi.org/10.18637/jss.v081.i10.

Neher, D. A. 2001. Role of nematodes in soil health and their use as indicators. Journal of Nematology 33(4):161-168.

Neher, D., T. Bongers, and H. Ferris. 2004. Computation of nematode community indices. Pp. 33 en Society of Nematologists Workshop. Vol. 2.

Ney, L., D. Franklin, K. Mahmud, M. Cabrera, D. Hancock, et al. 2019. Sensitivity of nematode community analysis to agricultural management practices and inoculation with local effective microorganisms in the Southeastern United States. Soil Syst 3(2):41. https://doi.org/10.3390/soilsystems3020041.

Okada, H., and H. Harada. 2007. Effects of tillage and fertilizer on nematode communities in a Japanese soybean field. Applied Soil Ecology 35(3):582-598. https://doi.org/10.1016/j.apsoil.2006.09.008.

Oksanen, J., G. L. Simpson, F. Guillaume Blanchet, R. Kindt, P. Legendre, et al. 2022. vegan: Community Ecology Package. R package versión 2.6-2.

Pan, F., R. Yan, J. Zhao, L. Li, Y. Hu, et al. 2022. Effects of grazing intensity on soil nematode community structure and function in different soil layers in a meadow steppe. Plant and Soil 471(1-2):33-46. https://doi.org/10.1007/s11104-021-05096-4.

Pan, F., N. Li, W. Zou, X. Han, and N. B. Mclaughlin. 2016. Soil nematode community structure and metabolic footprint in the early pedogenesis of a Mollisol. European Journal of Soil Biology 77:17-25. https://doi.org/10.1016/j.ejsobi.2016.09.004.

Pielou, E. C. 1969. An introduction to mathematical ecology. Bioscience 78(1):7-12.

QGIS Development Team. 2017. QGIS Geographic Information System. Open-Source Geospatial Foundation Project. URL: qgis.org.

R Core Team. 2022. R: A language and environment for statistical computing: R Foundation for Statistical Computing, Vienna, Austria. URL: R-project.org.

Ruf, A. 1998. A maturity index for predatory soil mites (Mesostigmata: Gamasina) as an indicator of environmental impacts of pollution on forest soils. Applied Soil Ecology 9(1):447-452. https://doi.org/10.1016/S0929-1393(98)00103-6.

Sae-Tun, O., G. Bodner, C. Rosinger, S. Zechmeister-Boltenstern, A. Mentler, et al. 2022. Fungal biomass and microbial necromass facilitate soil carbon sequestration and aggregate stability under different soil tillage intensities. Applied Soil Ecology 179:104599. https://doi.org/10.1016/j.apsoil.2022.104599.

Saikai, K., and A. E. MacGuidwin. 2022. Impact of Pratylenchus penetrans on soybeans grown in Wisconsin, USA. Plant Disease 106(11):2904-2910. https://doi.org/10.1094/PDIS-09-21-1888-RE.

Sánchez-Moreno, S., H. Minoshima, H. Ferris, and L. E. Jackson. 2006. Linking soil properties and nematode community composition: effects of soil management on soil food webs. Nematology 8(5):703-715. https://doi.org/10.1163/156854106778877857.

Sánchez-Moreno, S., S. Smukler, H. Ferris, A. T. O’geen, and L. E. Jackson. 2008. Nematode diversity, food web condition, and chemical and physical properties in different soil habitats of an organic farm. Biology and Fertility of Soils 44(5):727-744. https://doi.org/10.1007/s00374-007-0256-0.

Sánchez-Moreno, S., and M. Talavera. 2013. Los nematodos como indicadores ambientales en agroecosistemas. Revista Ecosistemas 22(1):50-55.

Sánchez-Moreno, S., and H. Ferris. 2018. Nematode ecology and soil health. Pp. 62-86 en R. A. Sikora, D. Coyne, J. Hallmann and P. Timper (eds.). Plant parasitic nematodes in subtropical and tropical agriculture. Wallingford UK: CAB International.

Schratzberger, M., M. Holterman, D. van Oevelen, and J. Helder. 2019. A worm’s world: Ecological flexibility pays off for free-living nematodes in sediments and soils. BioScience 69(11):867-876. https://doi.org/10.1093/biosci/biz086.

Siddiqi, M. R. 2000. Tylenchida: parasites of plants and insects. CABI, Wallingford, UK. Pp. 800. https://doi.org/10.1079/9780851992020.0000.

Sieriebriennikov, B., H. Ferris, and R. G. De Goede. 2014. NINJA: An automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology 61:90-93. https://doi.org/10.1016/j.ejsobi.2014.02.004.

Soto, R. L. 2016. Nematodes as soil quality indicators in coffee systems. MSc Thesis. Organic Agriculture - Farming System Ecology, Wageningen University. Pp. 53.

StatSoft, Inc. 2011. STATISTICA (data analysis software system), version 10. URL: statsoft.com.

Studdert, G. A. 2006. Rotaciones de cultivos en el sudeste de la provincia de Buenos Aires (Argentina): una herramienta para el manejo de la dinámica del nitrógeno y del carbono en el suelo. Tesis doctoral. Universitat de Lleida, Escola Tècnica Superior D’ Engiyeria Agrària. Lérida, Cataluña, España. Pp. 195.

Studdert, G. A., and H. E. Echeverría. 2002. Rotaciones mixtas, labranzas y carbono orgánico en la capa arable en el Sudeste bonaerense in Actas XVIII Congreso Argentino de la Ciencia del Suelo (CD). 16 - 19 de abril. Puerto Madryn, Chubut, Argentina. Asociación Argentina de la Ciencia del Suelo (AACS), Buenos Aires, Argentina.

Sun, F., K. Pan, A. Tariq, L. Zhang, X. Sun, et al. 2016. The response of the soil microbial food web to extreme rainfall under different plant systems. Sci Rep 6:37662. https://doi.org/10.1038/srep37662.

Swibawa, I. G., and T. N. Aeny. 2010. Nematode diversity in a range of land use types in Jambi Benchmark Indonesia. Jurnal Hama Dan Penyakit Tumbuhan Tropika 10(2):162-171. https://doi.org/10.23960/j.hptt.210162-171.

Tichy, L., and M. Chytry, M. 2006. Statistical determination of diagnostic species for site groups of unequal size. Journal of Vegetation science 17(6):809-818. https://doi.org/10.1111/j.1654-1103.2006.tb02504.x.

Tomazini, M. D., L. C. C. B. Ferraz, and A. R. Monteiro. 2008. Abundância e diversidade de nematóides em áreas contíguas de vegetação natural e submetida a diferentes tipos de uso do solo. Nematologia brasileira 32:185-193.

Treonis, A. M., E. H. Michelle, C. A. O’Leary, E. E. Austin, and C. B. Marks. 2010. Identification and localization of food-source microbial nucleic acids inside soil nematodes. Soil Biology and Biochemistry 42(11):2005-2011. https://doi.org/10.1016/j.soilbio.2010.07.026.

van den Boogaart, K. G., R. Tolosana-Delgado, and M. Bren. 2022. Compositions: Compositional Data Analysis. R package versión 2.0-4.

Vargas Gil, S., S. Benintende, S. Toresani, F. Covacevich, E. A. Mondino, et al. 2017. Biología de Suelos. Pp. 91-145 en D. J. Santos, M. G. Wilson and M. M. Ostinelli (eds.). Metodología de muestreo de suelo y ensayos a campo: Protocolos básicos comunes. 2° edición. Entre Rios, Ediciones INTA.

Videla, C., A. Pazos, P. C. Trivelin, H. E. Echeverría, and G. A. Studdert, G.A. 2005. Mineralización bruta de nitrógeno bajo labranza convencional, siembra directa y pastura. Ciencia del Suelo 23(2)1850-2067.

Volz, P. 1951. Untersuchungen über die Mikrofauna des Waldbodens. Zoologische Jahrbücher, Abteilung für Systematik, Ökologie und Geographie der Tiere 79:514-566.

Wang, K. H., P. Waisen, A. W. Leslie, R. Paudel, S. L. Meyer, et al. 2022. Relationships between Soil Tillage Systems, Nematode Communities and Weed Seed Predation. Horticulturae 8(5):425. https://doi.org/10.3390/horticulturae8050425.

Wickham, H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York, 2016. https://doi.org/10.1007/978-3-319-24277-4.

Yeates, G., T. Bongers, R. De Goede, D. Freckman, and S. Georgieva. 1993. Feeding habits in soil nematode families and genera-an outline for soil ecologists. Journal of Nematology 25(3):315-331.

Yeates, G., and T. Bongers. 1999. Nematode diversity in agroecosystems. Agriculture, Ecosystems and Environment 74(1):113-135. https://doi.org/10.1016/S0167-8809(99)00033-X.

Yeates, G. W. 2003. Nematodes as soil indicators: functional and biodiversity aspects. Biology and Fertility of Soils 37(4):199-210. https://doi.org/10.1007/s00374-003-0586-5.

Zhang, G., X. Sui, Y. Li, M. Jia, Z. Wang, et al. 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. https://doi.org/10.1007/s11368-019-02555-5.

Zhang, Y., S. Li, H. Li, R. Wang, K. Q. Zhang, et al. 2020. Fungi-nematode interactions: Diversity, ecology, and biocontrol prospects in agriculture. Journal of Fungi 6(4):206. https://doi.org/10.3390/jof6040206.

Zhao, J., and D. A. Neher. 2013. Soil nematode genera that predict specific types of disturbance. Applied Soil Ecology 64:135-141. https://doi.org/10.1016/j.apsoil.2012.11.008.

Zhong, S., H. C. Zeng, and Z. Q. Jin. 2017. Influences of different tillage and residue management systems on soil nematode community composition and diversity in the tropics. Soil Biology and Biochemistry 107:234-243. https://doi.org/10.1016/j.soilbio.2017.01.007.