Abstract
Aims
Plants can influence the level of herbivory experienced by neighboring plants. The importance of such belowground associational effects are poorly understood. In this study we examine whether Jacobaea vulgaris provides associational resistance against nematodes to neighboring plants.
Methods
Thirteen species (6 forbs, 3 grasses and 4 legumes) were each grown in mixtures with J. vulgaris and in monocultures. A nematode community was introduced to half of the pots. After 12 weeks, plant dry mass was assessed for each individual plant in each pot, and the number of nematodes in the soil and roots were identified. We then examined for each plant species its performance in mixtures and in monocultures, in presence and absence of nematodes and analyzed the abundance and composition of nematodes.
Results
Forbs produced more, grasses similar, and legumes less biomass in mixtures with J. vulgaris than in monocultures. Nematode addition did not influence biomass. There were fewer root-feeding nematodes in the soil in mixtures than in monocultures, but this was only true for plants that were good hosts for nematodes. The community composition of soil nematodes was different in monocultures and mixtures. Densities of migratory endoparasitic nematodes in the roots of neighboring plants were lower in mixtures than in monocultures. Moreover, the presence of nematodes changed the outcome of plant-plant interactions, often in favor of J. vulgaris.
Conclusions
Jacobaea vulgaris provides belowground associational resistance to other plants against migratory endoparasitic nematodes, and the presence of nematodes can change the outcome of plant-plant interactions.
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References
Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686. https://doi.org/10.1890/03-0650
Barbosa P, Hines J, Kaplan I et al (2009) Associational resistance and associational susceptibility: Having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. https://doi.org/10.1146/annurev.ecolsys.110308.120242
Barker KR (1998) Introduction and synopsis of advancements in nematology. In: Barker KR, Pederson GA, Windham GL, Bartels JM (eds) Plant and nematode interactions. American Society of Agronomy, Madison, pp 1–20
Bezemer TM, Fountain MT, Barea JM et al (2010) Divergent composition but similar function of soil food webs of individual plants: Plant species and community effects. Ecology 91:3027–3036. https://doi.org/10.1890/09-2198.1
Bongers T (1988) De Nematoden van Nederland. KNNV, Utrecht
Borgström P, Strengbom J, Marini L et al (2017) Above-and belowground insect herbivory modifies the response of a grassland plant community to nitrogen eutrophication. Ecology 98:545–554. https://doi.org/10.1002/ecy.1667
Borgström P, Strengbom J, Viketoft M, Bommarco R (2016) Aboveground insect herbivory increases plant competitive asymmetry, while belowground herbivory mitigates the effect. PeerJ 2016:e1867. https://doi.org/10.7717/peerj.1867
Brinkman EP, Duyts H, Karssen G et al (2015) Plant-feeding nematodes in coastal sand dunes: occurrence, host specificity and effects on plant growth. Plant Soil 397:17–30. https://doi.org/10.1007/s11104-015-2447-z
Brinkman EP, Duyts H, Van Der Putten WH (2005) Competition between endoparasitic nematodes and effect on biomass of Ammophila arenaria (marram grass) as affected by timing of inoculation and plant age. Nematology 7:169–178. https://doi.org/10.1163/1568541054879647
Cardinaux A, Hart SP, Alexander JM (2018) Do soil biota influence the outcome of novel interactions between plant competitors? J Ecol 106:1853–1863. https://doi.org/10.1111/1365-2745.13029
Carson WP, Root RB (2000) Herbivory and plant species coexistence: community regulation by an outbreaking phytophagous insect. Ecol Monogr 70:73–99. https://doi.org/10.1890/0012-9615(2000)070[0073:HAPSCC]2.0.CO;2
Craine JM, Wedin DA, Iii FSC, Reich PB (2002) Relationship between the structure of root systems and resource use for 11 North American grassland plants. Plant Ecol 165:85–100. https://doi.org/10.1023/A:1021414615001
Davis EL, Mitchum MG (2005) Nematodes. Sophisticated parasites of legumes. Plant Physiol 137:1182–1188. https://doi.org/10.1104/pp.104.054973
De Deyn GB, Raaijmakers CE, Van Ruijven J et al (2004) Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web. Oikos 106:576–586. https://doi.org/10.1111/j.0030-1299.2004.13265.x
De Deyn GB, Raaijmakers CE, Zoomer HR et al (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713. https://doi.org/10.1038/nature01548
de la Peña E, Bonte D, Moens M (2009) Evidence of population differentiation in the dune grass Ammophila arenaria and its associated root-feeding nematodes. Plant Soil 324:307–316. https://doi.org/10.1007/s11104-009-9958-4
de Matos C da C, Monteiro LCP, Gallo SAD, et al (2019) Changes in soil microbial communities modulate interactions between maize and weeds. Plant Soil 440:249–264. https://doi.org/10.1007/s11104-019-04066-1
Elhady A, Adss S, Hallmann J, Heuer H (2018) Rhizosphere microbiomes modulated by pre-crops assisted plants in defense against plant-parasitic nematodes. Front Microbiol 9:1133. https://doi.org/10.3389/fmicb.2018.01133
Fransen B, Blijjenberg J, De Kroon H (1999) Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant Soil 211:179–189. https://doi.org/10.1023/A:1004684701993
Fransen B, de Kroon H, Berendse F (1998) Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115:351–358. https://doi.org/10.1007/s004420050527
Fraser LH, Grime JP (1999) Interacting effects of herbivory and fertility on a synthesized plant community. J Ecol 87:514–525. https://doi.org/10.1046/j.1365-2745.1999.00373.x
Fry EL, Evans AL, Sturrock CJ et al (2018) Root architecture governs plasticity in response to drought. Plant Soil 433:189–200. https://doi.org/10.1007/s11104-018-3824-1
Graff P, Aguiar MR (2011) Testing the role of biotic stress in the stress gradient hypothesis. Processes and patterns in arid rangelands. Oikos 120:1023–1030. https://doi.org/10.1111/j.1600-0706.2010.19059.x
Haag JJ, Coupe MD, Cahill JF (2004) Antagonistic interactions between competition and insect herbivory on plant growth. J Ecol 92:156–167. https://doi.org/10.1111/j.1365-2745.2004.00847.x
Harkes P, Verhoeven A, Sterken MG et al (2017) The differential impact of a native and a non-native ragwort species (Senecioneae) on the first and second trophic level of the rhizosphere food web. Oikos 126:1790–1803. https://doi.org/10.1111/oik.04530
Harper JL, Wood WA (1957) Senecio Jacobaea L. J Ecol 45:617–637. https://doi.org/10.2307/2256946
Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science (80- ) 324:636–638. https://doi.org/10.1126/science.1169640
He L, Xu J, Hu L et al (2019) Nurse effects mediated by acid-tolerance of target species and arbuscular mycorrhizal colonization in an acid soil. Plant Soil 441:161–172. https://doi.org/10.1007/s11104-019-04103-z
Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: Root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22:811–820. https://doi.org/10.1046/j.1365-3040.1999.00454.x
Hol WHG, de Boer W, Termorshuizen AJ et al (2010) Reduction of rare soil microbes modifies plant-herbivore interactions. Ecol Lett 13:292–301. https://doi.org/10.1111/j.1461-0248.2009.01424.x
Hol WHG, Macel M, Van Veen JA, Van Der Meijden E (2004) Root damage and aboveground herbivory change concentration and composition of pyrrolizidine alkaloids of Senecio jacobaea. Basic Appl Ecol 5:253–260. https://doi.org/10.1016/j.baae.2003.12.002
Hothorn T, Bretz F, Westfall P (2008) Simultaneous Inference in General Parametric Models. Biometrical J 50:346–363. https://doi.org/10.1002/bimj.200810425
Huang W, Gfeller V, Erb M (2019) Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants. Plant Cell Environ 42:1964–1973. https://doi.org/10.1111/pce.13534
Jing J, Bezemer TM, van der Putten WH (2015a) Interspecific competition of early successional plant species in ex-arable fields as influenced by plant-soil feedback. Basic Appl Ecol 16:112–119. https://doi.org/10.1016/j.baae.2015.01.001
Jing J, Raaijmakers C, Kostenko O et al (2015b) Interactive effects of above- and belowground herbivory and plant competition on plant growth and defence. Basic Appl Ecol 16:500–509. https://doi.org/10.1016/j.baae.2015.04.009
Johnson SN, Benefer CM, Frew A et al (2016a) New frontiers in belowground ecology for plant protection from root-feeding insects. Appl Soil Ecol 108:96–107. https://doi.org/10.1016/j.apsoil.2016.07.017
Johnson SN, Erb M, Hartley SE (2016b) Roots under attack: contrasting plant responses to below- and aboveground insect herbivory. New Phytol 210:413–418. https://doi.org/10.1111/nph.13807
Kaplan I, Halitschke R, Kessler A et al (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406. https://doi.org/10.1890/07-0471.1
Kaplan I, Sardanelli S, Denno RF (2009) Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecol Entomol 34:262–270. https://doi.org/10.1111/j.1365-2311.2008.01062.x
Kassambara A (2021) rstatix: Pipe-Friendly Framework for Basic Statistical Tests. R package version 0.7.0. https://CRAN.R-project.org/package=rstatix
Kim TN, Underwood N, Inouye BD (2013) Insect herbivores change the outcome of plant competition through both inter- and intraspecific processes. Ecology 94:1753–1763. https://doi.org/10.1890/12-1261.1
Körner K, Pfestorf H, May F, Jeltsch F (2014) Modelling the effect of belowground herbivory on grassland diversity. Ecol Modell 273:79–85. https://doi.org/10.1016/j.ecolmodel.2013.10.025
Kos M, Bukovinszky T, Mulder PPJ, Bezemer TM (2015) Disentangling above- and belowground neighbor effects on the growth, chemistry, and arthropod community on a focal plant. Ecology 96:164–175. https://doi.org/10.1890/14-0563.1
Kostenko O, Mulder PPJ, Bezemer TM (2013) Effects of Root Herbivory on Pyrrolizidine Alkaloid Content and Aboveground Plant-Herbivore-Parasitoid Interactions in Jacobaea Vulgaris. J Chem Ecol 39:109–119. https://doi.org/10.1007/s10886-012-0234-3
Kostenko O, Mulder PPJ, Courbois M, Bezemer TM (2016) Effects of plant diversity on the concentration of secondary plant metabolites and the density of arthropods on focal plants in the field. J Ecol 105:647–660. https://doi.org/10.1111/1365-2745.12700
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. https://doi.org/10.1007/s004420100716
Lepik A, Abakumova M, Davison J et al (2020) Spatial mapping of root systems reveals diverse strategies of soil exploration and resource contest in grassland plants. J Ecol 109:652–663. https://doi.org/10.1111/1365-2745.13535
Lin T, Klinkhamer PGL, Vrieling K (2018) Evolutionary changes in growth, regrowth and carbohydrate storage in an invasive plant. Sci Rep 8:14917. https://doi.org/10.1038/s41598-018-33218-z
Louthan AM, Doak DF, Goheen JR, Palmer TM, Pringle RM (2014) Mechanisms of plant-plant interactions: concealment from herbivores is more important than abiotic-stress mediation in an African savannah. Proc Royal Soc B 281:20132647. https://doi.org/10.1098/rspb.2013.2647
Macel M (2011) Attract and deter: A dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochem Rev 10:75–82. https://doi.org/10.1007/s11101-010-9181-1
Moens M, Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annu Rev Phytopathol 47:313–332. https://doi.org/10.1146/annurev-phyto-080508-081846
Niemelä M, Markkola A, Mutikainen P (2008) Modification of competition between two grass species by a hemiparasitic plant and simulated grazing. Basic Appl Ecol 9:117–125. https://doi.org/10.1016/j.baae.2007.01.001
Oduor AMO, Stift M, Van Kleunen M (2015) The interaction between root herbivory and competitive ability of native and invasive-range populations of Brassica nigra. PLoS ONE 10:e0141857. https://doi.org/10.1371/journal.pone.0141857
Oduor AMO, van Kleunen M, Stift M (2017) In the presence of specialist root and shoot herbivory, invasive-range Brassica nigra populations have stronger competitive effects than native-range populations. J Ecol 105:1679–1686. https://doi.org/10.1111/1365-2745.12779
Oksanen J, Blanchet FG, Friendly M et al (2019) vegan: Community Ecology Package. R package version 2.5-5. https://CRAN.R-project.org/package=vegan. Community Ecol Packag 2
Oostenbrink M (1960) The family Criconematidae. In: Sasser JN, Jenkins WR (eds) Nematology fundamentals and recent advances with emphasis on plant parasitic and soil forms. The University of North Carolina Press, Chapel Hill, pp 196–205
Pinheiro J, Bates D, DebRoy S et al (2019) nlme: Linear and nonlinear mixed effects models. https://cran.r-project.org/package=nlme.R-project
Piśkiewicz AM, Duyts H, van der Putten WH (2008) Multiple species-specific controls of root-feeding nematodes in natural soils. Soil Biol Biochem 40:2729–2735. https://doi.org/10.1016/j.soilbio.2008.07.006
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Ramsell J, Malloch AJC, Whittaker JB (1993) When grazed by Tipula Paludosa, Lolium Perenne is a stronger competitor of Rumex Obtusifolius. J Ecol 81:777. https://doi.org/10.2307/2261675
Rasmann S, Agrawal AA (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875–880. https://doi.org/10.1104/pp.107.112045
Ravenek JM, Mommer L, Visser EJW et al (2016) Linking root traits and competitive success in grassland species. Plant Soil 407:39–53. https://doi.org/10.1007/s11104-016-2843-z
Rees M, Brown VK (1992) Interactions between invertebrate herbivores and plant competition. J Ecol 80:353. https://doi.org/10.2307/2261017
Schädler M, Brandl R, Haase J (2007) Antagonistic interactions between plant competition and insect herbivory. Ecology 88:1490–1498. https://doi.org/10.1890/06-0647
Scheublin TR, Van Logtestijn RSP, Van Der Heijden MGA (2007) Presence and identity of arbuscular mycorrhizal fungi influence competitive interactions between plant species. J Ecol 95:631–638. https://doi.org/10.1111/j.1365-2745.2007.01244.x
Schouteden N, De WD, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280
Sikder MM, Vestergård M (2020) Impacts of root metabolites on soil nematodes. Front Plant Sci 10:1792. https://doi.org/10.3389/fpls.2019.01792
Stein C, Unsicker SS, Kahmen A et al (2010) Impact of invertebrate herbivory in grasslands depends on plant species diversity. Ecology 91:1639–1650. https://doi.org/10.1890/09-0600.1
Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346. https://doi.org/10.1007/BF00345736
Thoden TC, Boppré M (2010) Plants producing pyrrolizidine alkaloids: Sustainable tools for nematode management? Nematology 12:1–24. https://doi.org/10.1163/138855409X12549869072248
Thoden TC, Boppré M, Hallmann J (2009a) Effects of pyrrolizidine alkaloids on the performance of plant-parasitic and free-living nematodes. Pest Manag Sci 65:823–830. https://doi.org/10.1002/ps.1764
Thoden TC, Hallmann J, Boppré M (2009b) Effects of plants containing pyrrolizidine alkaloids on the northern root-knot nematode Meloidogyne hapla. Eur J Plant Pathol 123:27–36. https://doi.org/10.1007/s10658-008-9335-9
Underwood N, Inouye BD, Hambäck PA (2014) A conceptual framework for associational effects: when do neighbors matter and how would we know? Q Rev Biol 89:1–19. https://doi.org/10.1086/674991
Van de Voorde TFJ, Van der Putten WH, Bezemer TM (2012) The importance of plant-soil interactions, soil nutrients, and plant life history traits for the temporal dynamics of Jacobaea vulgaris in a chronosequence of old-fields. Oikos 121:1251–1262. https://doi.org/10.1111/j.1600-0706.2011.19964.x
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Verschoor BC, Pronk TE, De Goede RGM, Brussaard L (2002) Could plant-feeding nematodes affect the competition between grass species during succession in grasslands under restoration management? J Ecol 90:753–761. https://doi.org/10.1046/j.1365-2745.2002.00710.x
Viketoft M, Palmborg C, Sohlenius B et al (2005) Plant species effects on soil nematode communities in experimental grasslands. Appl Soil Ecol 30:90–103. https://doi.org/10.1016/j.apsoil.2005.02.007
Voglar GE, Mrak T, Križman M et al (2019) Effect of contaminated soil on multitrophic interactions in a terrestrial system. Plant Soil 435:337–351. https://doi.org/10.1007/s11104-018-03903-z
Wang M, De Deyn GB, Bezemer TM (2019) Separating effects of soil microorganisms and nematodes on plant community dynamics. Plant Soil 441:455–467. https://doi.org/10.1007/s11104-019-04137-3
White JA, Andow DA (2006) Habitat modification contributes to associational resistance between herbivores. Oecologia 148:482–490. https://doi.org/10.1007/s00442-006-0388-1
Wurst S, Rillig MC (2011) Additive effects of functionally dissimilar above-and belowground organisms on a grassland plant community. J Plant Ecol 4:221–227. https://doi.org/10.1093/jpe/rtr012
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
Ye Y, Rui Y, Zeng Z, et al (2020) Responses of soil nematode community to monoculture or mixed culture of a grass and a legume forage species in China. Pedosphere 30:791–800. https://doi.org/10.1016/S1002-0160(20)60039-X
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X.Y.L. was funded by a Chinese Scholarship Council (CSC) grant. We thank four anonymous reviewers for their insightful comments and helpful suggestions.
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T.M.B designed the experiment. C.R. maintained the experiment and extracted and identified nematodes and C.R. and T.M.B. collected biomass data. X.Y.L, K.V. and S.T.E.L. and T.M.B. developed and discussed analysis and presentation of the data, and X.Y.L analyzed all data. X.Y.L. and T.M.B. wrote the first version of the manuscript; and all authors revised and improved subsequent versions of the manuscript.
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Liu, X., Raaijmakers, C., Vrieling, K. et al. Associational resistance to nematodes and its effects on interspecific interactions among grassland plants. Plant Soil 471, 591–607 (2022). https://doi.org/10.1007/s11104-021-05238-8
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DOI: https://doi.org/10.1007/s11104-021-05238-8