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Can root traits predict communities of soil nematodes in restored northern prairies?

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Abstract

Aims

We examined how restoration affects the structure and function of grasslands belowground by relating changes in the morphology and architecture of root systems of dominant plants to the structure of soil food webs.

Methods

We measured changes in root traits of dominant plants (Bouteloua gracilis and Pascopyrum smithii) and related them to the diversity and feeding structure of soil nematodes across a restoration chronosequence in a mixed-grass prairie in Grasslands National Park, Saskatchewan, Canada.

Results

Root architecture and morphology of dominant grasses changed with restoration, and soil food webs in recently restored prairies centred around resources provided by roots. In contrast, food webs in a native prairie centred around the decomposition of soil organic matter and plant litter.

Conclusions

Our study demonstrates that changes in root traits following restoration can cascade through soil foodwebs, altering the function of restored prairies. Our study also highlights that the diversity and structure of soil nematodes can reflect changes in root traits of dominant plants. However, traits that generalize the whole root system may be insufficient to explain the causal relationship between root feeding nematodes and their resources.

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References

  • Atkinson RRL, Burrell MM, Osborne CP, Rose KE, Rees M (2012) A non-targeted metabolomics approach to quantifying differences in root storage between fast- and slow-growing plants. New Phytol 196:200–211

    CAS  PubMed  Google Scholar 

  • Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699

    PubMed  Google Scholar 

  • Barker KR, Carter CC, Sasser JN (1985) An advanced treatise on Meloidogyne: methodology. North Carolina State University: Department of Plant Pathology

  • Belter PR, Cahill JF (2015) Disentangling root system responses to neighbours: identification of novel root behavioural strategies. AoB Plants 7:1–12

    CAS  Google Scholar 

  • Bongers T (1988) De Nematoden van Nederland. Pirola, Schoorl: KNNV-bibliotheekuitgave 46

  • Caplan JS, Meiners SJ, Flores-Moreno H, McCormack ML (2019) Fine-root traits are linked to species dynamics in a successional plant community. Ecology 100:e02588

    PubMed  Google Scholar 

  • Coffey V, Otfinowski R (2019) Legacies of afforestation on soil nematode community composition, structure, and diversity in a northern Canadian prairie. Plant Soil 435:437–447

    CAS  Google Scholar 

  • Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727

    Google Scholar 

  • Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerling DJ (2012) Evolutionary patterns and biogeochemical significance of angiosperm root traits. Int J Plant Sci 173:584–595

    Google Scholar 

  • Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Google Scholar 

  • Cortois R, Veen GF(C), Duyts H, Abbas M, Strecker T, Kostenko O, Eisenhauer N, Scheu S, Gleixner G, Deyn GBD et al (2017) Possible mechanisms underlying abundance and diversity responses of nematode communities to plant diversity. Ecosphere 8:e01719

    Google Scholar 

  • Craine JM, Froehle J, Tilman DG, Wedin DA, Chapin IFS (2001) The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos 93:274–285

    Google Scholar 

  • Cui M, Caldwell MM (1997) A large ephemeral release of nitrogen upon wetting of dry soil and corresponding root responses in the field. Plant Soil 191:219–299

    Google Scholar 

  • Davies MG, Gray A (2015) Don’t let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecol Evol 5:5295–5304

    PubMed  PubMed Central  Google Scholar 

  • De Deyn GB, Cornelissen JHC, Bardgett RD (2008) Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol Lett 11:516–531

    PubMed  Google Scholar 

  • de Vries FT, Brown C, Stevens CJ (2016) Grassland species root response to drought: consequences for soil carbon and nitrogen availability. Plant Soil 409:297–312

    Google Scholar 

  • Delgado NJ, Casler MD, Grau CR, Jung HG (2002) Reactions of smooth bromegrass clones with divergent lignin or etherified ferulic acid concentration to three fungal pathogens. Crop Sci 42:1824–1831

    Google Scholar 

  • Deyn GBD, Raaijmakers CE, Ruijven JV, Berendse F, Putten WHVD (2004) Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106:576–586

    Google Scholar 

  • Eisenhauer N, Migunova VD, Ackermann M, Ruess L, Scheu S (2011) Changes in plant species richness induce functional shifts in soil nematode communities in experimental grassland. PLoS One 6

  • Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep 7:44641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42

    CAS  Google Scholar 

  • Elsen A, Beeterens R, Swennen R, De Waele D (2003) Effects of an arbuscular mycorrhizal fungus and two plant-parasitic nematodes on Musa genotypes differing in root morphology. Biol Fertil Soils 38:367–376

    Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL et al (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    CAS  PubMed  Google Scholar 

  • Environment and Climate Change Canada (2013) Climate normals 1981–2010 station data: Val-Marie. URL https://climate.weather.gc.ca/climate_normals/results_1981_2010_e.html?stnID=3196andautofwd=1. [Accessed 27 Nov 2019]

  • Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu W, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao J, Cornelissen JHC (2013) Linking litter decomposition of above- and below-ground organs to plant–soil feedbacks worldwide. J Ecol 101:943–952

    CAS  Google Scholar 

  • Gardner WH (1986) Water content. In Methods of soil analysis: part 1: physical and mineralogical methods (ed. A. Klute). Madison, Wisconsin: Soil Science Society of America

  • Goodall DW (1952) Some considerations in the use of point quadrats for the analysis of vegetation. Aust J Biol Sci 5:1–41

    CAS  Google Scholar 

  • Great Plains Flora Association (1986) Flora of the Great Plains. University Press of Kansas, Lawrence

    Google Scholar 

  • Hecht VL, Temperton VM, Nagel KA, Rascher U, Pude R, Postma JA (2018) Plant density modifies root system architecture in spring barley (Hordeum vulgare L.) through a change in nodal root number. Plant Soil 439:179–200

    Google Scholar 

  • Hishi T (2007) Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions. J For Res 12:126–133

    Google Scholar 

  • Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. J Ecol 99:954–963

    Google Scholar 

  • Hu J, Wu J, Ma M, Nielsen UN, Wang J, Du G (2015) Nematode communities response to long-term grazing disturbance on Tibetan plateau. Eur J Soil Biol 69:24–32

    Google Scholar 

  • Hutchings MJ, John EA (2003) Distribution of roots in soil, and root foraging activity. In Root ecology Heidelberg: Springer-Verlag p 33–60

  • Ingham ER, Trofymow JA, Ames RN, Hunt HW, Morley CR, Moore JC, Coleman DC (1986) Trophic interactions and nitrogen cycling in a semi-arid grassland soil. i. Seasonal dynamics of the natural populations, their interactions and effects on nitrogen cycling. J Appl Ecol 23:597–614

    Google Scholar 

  • Jairajpuri MS, Ahmad W (1992) Dorylaimida: free-living, predaceous and plant-parasitic nematodes. E.J. Brill, Leiden

    Google Scholar 

  • Jiang Y, Qian H, Wang X, Chen L, Liu M, Li H, Sun B (2018) Nematodes and microbial community affect the sizes and turnover rates of organic carbon pools in soil aggregates. Soil Biol Biochem 119:22–31

    CAS  Google Scholar 

  • Kämpf I, Mathar W, Kuzmin I, Hölzel N, Kiehl K (2016) Post-soviet recovery of grassland vegetation on abandoned fields in the forest steppe zone of Western Siberia. Biodivers Conserv 25:2563–2580

    Google Scholar 

  • Kardol P, Wardle DA (2010) How understanding aboveground–belowground linkages can assist restoration ecology. Trends Ecol Evol 25:670–679

    PubMed  Google Scholar 

  • Kardol P, Bezemer TM, van der Wal A, van der Putten WH (2005) Successional trajectories of soil nematode and plant communities in a chronosequence of ex-arable lands. Biol Conserv 126:317–327

    Google Scholar 

  • Kembel SW, De Kroon H, Cahill JF, Mommer L (2008) Improving the scale and precision of hypotheses to explain root foraging ability. Ann Bot 101:1295–1301

    PubMed  PubMed Central  Google Scholar 

  • Koebernick N, Daly KR, Keyes SD, Bengough AG, Brown LK, Cooper LJ, George TS, Hallett PD, Naveed M, Raffan A et al (2019) Imaging microstructure of the barley rhizosphere: particle packing and root hair influences. New Phytol 221:1878–1889

    PubMed  Google Scholar 

  • Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310

    Google Scholar 

  • Krusberg LR, Nielsen LW (1958) Pathogenesis of root-knot nematodes to the Puerto Rico variety of sweet potato. Phytopathology 48:30–39

    Google Scholar 

  • Laliberté E (2017) Below-ground frontiers in trait-based plant ecology. New Phytol 213:1597–1603

    PubMed  Google Scholar 

  • Lauenroth WK, Gill R (2003) Turnover of root systems. In: de Kroon H, Visser EJW (eds) Root ecology. Springer-Verlag, Berlin, pp 61–89

    Google Scholar 

  • Legendre P, Legendre LFJ (2012) Numerical Ecology. Elsevier, Oxford

    Google Scholar 

  • Lindford MB (1939) Attractiveness of roots and excised shoot tissues to certain nematodes. Proc Helminthol Soc Wash 6:8–11

    Google Scholar 

  • Maynard DG, Kalra YP (1993) Nitrate and exchangeable ammonium nitrogen. In: Carter MR (ed) Soil sampling and methods of analysis. CRC Press, Boca Raton

    Google Scholar 

  • McCormack ML, Iversen CM (2019) Physical and functional constraints on viable belowground acquisition strategies. Front Plant Sci 10

  • McCormack ML, Guo D, Iversen CM, Chen W, Eissenstat DM, Fernandez CW, Li L, Ma C, Ma Z, Poorter H et al (2017) Building a better foundation: improving root-trait measurements to understand and model plant and ecosystem processes. New Phytol 215:27–37

    PubMed  Google Scholar 

  • Morriën E, Hannula SE, Snoek LB, Helmsing NR, Zweers H, de Hollander M, Soto RL, Bouffaud M-L, Buée M, Dimmers W et al (2017) Soil networks become more connected and take up more carbon as nature restoration progresses. Nat Commun 8:1–10

    Google Scholar 

  • Mueller KE, Blumenthal DM, Carrillo Y, Cesarz S, Ciobanu M, Hines J, Pabst S, Pendall E, de Tomasel CM, Wall DH et al (2016) Elevated CO2 and warming shift the functional composition of soil nematode communities in a semiarid grassland. Soil Biol Biochem 103:46–51

    Google Scholar 

  • Nelson DW, Sommers LE (1996) Chapter 34: Total carbon, organic carbon, and organic matter. In: Sparks DL (ed) Methods of soil analysis: part 3 - chemical methods. Soil Science Society of America and American Society of Agronomy, Madison

    Google Scholar 

  • Nobel PS (1994) Root-soil responses to water pulses in dry environments. In: Caldwell MM, Pearcy RW (eds) Exploitation of environmental heterogeneity by plants: ecophysiological processes above- and belowground. Academic press, San Diego, pp 285–304

    Google Scholar 

  • Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, et al. (2019) Vegan: community ecology package. R package version 2.5–4. https://CRAN.R-project.org/package=vegan [Accessed 13 March 2019]

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Department of Agriculture circular 939

  • Parks Canada (2010) Grasslands National Park of Canada management plan. 79 pp

  • Pinno BD, Wilson SD (2013) Fine root response to soil resource heterogeneity differs between grassland and forest. Plant Ecol 214:821–829

    Google Scholar 

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. URL https://www.R-project.org/ [Accessed 13 March 2019]

  • Rasmann S, Bauerle TL, Poveda K, Vannette R (2011) Predicting root defence against herbivores during succession. Funct Ecol 25:368–379

    Google Scholar 

  • Ravenek JM, Mommer L, Visser EJW, van Ruijven J, van der Paauw JW, Smit-Tiekstra A, de Caluwe H, de Kroon H (2016) Linking root traits and competitive success in grassland species. Plant Soil 407:39–53

    CAS  Google Scholar 

  • Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Google Scholar 

  • Ritz K, Black HIJ, Campbell CD, Harris JA, Wood C (2009) Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecol Indic 9:1212–1221

    CAS  Google Scholar 

  • Rose L (2017) Pitfalls in root trait calculations: how ignoring diameter heterogeneity can lead to overestimation of functional traits. Front Plant Sci 8:1–5

    Google Scholar 

  • Rosseel Y (2012) Lavaan: an R package for structural equation modeling. J Stat Softw 48:1–36

    Google Scholar 

  • Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Cao K, Stokes A (2016) Root structure–function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210:815–826

    PubMed  Google Scholar 

  • Ryser P (1996) The importance of tissue density for growth and life span of leaves and roots: a comparison of five ecologically contrasting grasses. Funct Ecol 10:717–723

    Google Scholar 

  • Saskatchewan Institute of Pedology (1992) The soils of Val Marie. Rural Municipality No. 17. Saskatchewan. Centre for Land and Biological Resources Research, Land Resources Division, Agriculture Canada. Publication 92–51

  • Shipley B (2016) Cause and correlation in bBiology: a user’s guide to path analysis, structural equations and causal inference with R. 2nd ed. Cambridge University Press, Cambridge

  • Shipley B (2017) CauseAndCorrelation: functions for path analysis and SEM. R package version 0.1. http://github.com/BillShipley/CauseAndCorrelation [Accessed 3 May 2019]

  • Shipley B, Vile D, Garnier E (2006) From plant traits to plant communities: a statistical mechanistic approach to biodiversity. Science 314:812–814

    CAS  PubMed  Google Scholar 

  • Shipley B, Bello FD, Cornelissen JHC, Laliberté E, Laughlin DC, Reich PB (2016) Reinforcing loose foundation stones in trait-based plant ecology. Oecologia 180:923–931

    PubMed  Google Scholar 

  • Thorpe J, Baldwin K, Allen L (2015) Great Plains Mixedgrass prairie. Sault Ste. Marie, Ontario, Canada: Canadian National Vegetation Classification Macrogroup. http://cnvc-cnvc.ca/index.cfm [Accessed 17 June 2017]

  • Tierney GL, Fahey TJ (2007) Estimating belowground primary productivity. In: Fahey TJ, Knapp AK (eds) Principles and standards for measuring primary production. Oxford University Press, Oxford, pp 120–141

    Google Scholar 

  • Tsunoda T, van Dam NM (2017) Root chemical traits and their roles in belowground biotic interactions. Pedobiologia 65:58–67

    Google Scholar 

  • van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265

    PubMed  Google Scholar 

  • Verschoor BC, de Goede RGM, Brussaard L (2002) Do plant parasitic nematodes have differential effects on the productivity of a fast- and a slow-growing grass species? Plant Soil 243:81–90

    CAS  Google Scholar 

  • Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252

    PubMed  Google Scholar 

  • Wall-Freckman D, Huang SP (1998) Response of the soil nematode community in a shortgrass steppe to long-term and short-term grazing. Appl Soil Ecol 9:39–44

    Google Scholar 

  • Wang K-H, McSorley R, Bohlen P, Gathumbi SM (2006) Cattle grazing increases microbial biomass and alters soil nematode communities in subtropical pastures. Soil Biol Biochem 38:1956–1965

    CAS  Google Scholar 

  • Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169

    CAS  PubMed  Google Scholar 

  • 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. J Nematol 25:315–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou M, Bai W, Zhang Y, Zhang W-H (2018) Multi-dimensional patterns of variation in root traits among coexisting herbaceous species in temperate steppes. J Ecol 106:2320–2331

    Google Scholar 

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Acknowledgements

The help of A-C Olivier in the field and the lab is particularly acknowledged, as is the support of Parks Canada staff, including M. Sliwinski, S. Liccioli, D. Grant, and C. Schmidt. We gratefully acknowledge helpful discussions with Benjamin Delory, Bill Shipley, and Arinawa Liz Del Prado Filartiga, as well as the helpful comments from four anonymous reviewers.

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  1. Department of Biology, University of Winnipeg, 515 Portage Avenue, Winnipeg, MB, R3B 2E9, Canada

    Rafael Otfinowski & Victory Coffey

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  1. Rafael Otfinowski
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  2. Victory Coffey
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RO conceptualized, designed, and acquired funding for the research; RO and VC performed the research, collected, analyzed, and interpreted the data, and wrote the manuscript.

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Correspondence to Rafael Otfinowski.

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Otfinowski, R., Coffey, V. Can root traits predict communities of soil nematodes in restored northern prairies?. Plant Soil 453, 459–471 (2020). https://doi.org/10.1007/s11104-020-04624-y

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