Skip to main content
SpringerLink
Log in

What happens next? Legacy effects induced by grazing and grass-endophyte symbiosis on thistle plants and their floral visitors

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Complex webs of multiple interactions determine the final aboveground and belowground community structure. While the mechanisms are difficult to determine, soil conditioning may modify other plants performance and their interaction with other organisms. We aim to determine the extent to which aboveground Epichloë endophytes and consumers induce legacy effects on subsequent plants and their interactions with floral visitors.

Methods

We performed two mesocosm experiments in two phases. Firstly, annual ryegrass plants (Lolium multiflorum), in symbiosis or not with Epichloë occultans and subjected or not to grazing, were grown in mesocoms to generate four soil conditionings. Secondly, thistle plants (Carduus acanthoides) were grown in these conditioned soils. We assessed thistle plants aerial biomass, number of flower heads and their floral visitors.

Results

The presence of one or both interactions (symbiosis and grazing) reduced total visits in subsequent thistle plants by 45 %. In particular, honeybees and other bees were reduced by 42 and 51 %, respectively. The flower head number or biomass of thistle plants may only partially mediate these effects.

Conclusions

To better understand the rules structuring communities and ecological processes, it is critical to connect multiple interactions effects on soil conditions and their influence on trophic and non-trophic interactions during the subsequent generations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

E+:

Seeds of annual ryegrass (Lolium multiflorum) with high incidence of endophyte Epichloë occultans

E-:

Seeds of annual ryegrass (L. multiflorum) with low incidence of endophyte E. occultans

G+:

L. multiflorum population subject to simulated grazing

G-:

L. multiflorum population do not subject to simulated grazing

Corg:

Soil organic carbon

Nt:

Soil total nitrogen

das:

Days after seeding

ISTA:

International seed testing association

References

  • Arechavaleta M, Bacon CW, Plattner RD et al (1992) Accumulation of ergopeptide alkaloids in symbiotic tall fescue grown under deficits of soil water and nitrogen fertilizer. Appl Environ Microbiol 58:857–861

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159

    Article  CAS  PubMed  Google Scholar 

  • Bais HP, Broeckling CD, Vivanco JM (2008) Root exudates modulate plant—microbe interactions in the rhizosphere. Second. Metab. soil Ecol. Springer Berlin Heidelber, pp 241–252

  • Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878. doi:10.1016/S0038-0717(98)00069-8

  • Bates D, Maechler M, Bolker B et al (2014) lme4: Linear mixed-effects models using Eigen and S4 Maintainer. 1:1–7

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Article  Google Scholar 

  • Bolker B, Team RDC (2014) bbmle: tools for general maximum likelihood estimation. R Packag. version 1.0.17

  • Bolker BM, Brooks ME, Clark CJ et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol (Personal Ed 24:127–35. doi: 10.1016/j.tree.2008.10.008

  • Bolker B, Skaug H, Magnusson A, Nielsen A (2013) Getting started with the glmmADMB package. 1–17

  • Brown VK, Gange AC (1992) Secondary plant succession: how is it modified by insect herbivory? Vegetatio 101:3–13

    Article  Google Scholar 

  • Bultman TL, Bell G, Martin WD (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685

    Article  Google Scholar 

  • Cahill JF, Elle E, Smith GR, Shore BH (2008) Disruption of a belowground mutualism alers interactions between palnts and their floral visitors. Ecology 89:1791–1801

    Article  PubMed  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons : invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965

    Article  Google Scholar 

  • Callaway RM, Cipollini D, Barto K et al (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Eupore. Ecology 89:1043–1055

    Article  PubMed  Google Scholar 

  • Casanova-Katny MA, Torres-Mellado GA, Palfner G, Cavieres LA (2011) The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21:613–622. doi:10.1007/s00572-011-0367-1

    Article  PubMed  Google Scholar 

  • Casas C, Omacini M, Montecchia MS, Correa OS (2011) Soil microbial community responses to the fungal endophyte Neotyphodium in Italian ryegrass. Plant Soil 340:347–355. doi:10.1007/s11104-010-0607-8

    Article  CAS  Google Scholar 

  • Cheplick GP, Faeth SH (2009) Ecology and evolution of the grass-endophyte symbiosis. Oxford University ress, New York

    Book  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16. doi:10.2307/1943155

    Article  Google Scholar 

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285(5434):1742–1744

    Article  CAS  PubMed  Google Scholar 

  • Clay K, Schardl CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:99–127

    Article  Google Scholar 

  • Cragg RG, Bardgett RD (2010) How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biol 33:2073–2081

    Article  Google Scholar 

  • Culman SW, DuPont ST, Glover JD et al (2010) Agriculture, ecosystems and environment long-term impacts of high-input annual cropping and unfertilized perennial grass production on soil properties and belowground food webs in Kansas, USA. Agric Ecosyst Environ 137:13–24. doi:10.1016/j.agee.2009.11.008

    Article  Google Scholar 

  • De Battista J (2005) Neotyphodium research and aplication in South America. In: Roberts CA, West CP, Spiers DE (eds) Neotyphodium cool. Grasses, 1st edn. Blackwell Publishing Ldt, Oxford, pp 65–71

    Chapter  Google Scholar 

  • De Deyn GB, Raaijmakers CE, Zoomer HR et al (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713

    Article  PubMed  Google Scholar 

  • Desrochers AM, Bain JF, Warwick SI (1988) The biology of Canadian weeds: Carduus nutans L. and Carduus acanhoides L. Can J Plant Sci 68:1053–1068

    Article  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. Vienna, Austria

  • Druille M, Omacini M, Golluscio RA, Cabello MN (2013) Arbuscular mycorrhizal fungi are directly and indirectly affected by glyphosate application. Appl Soil Ecol 72:143–149. doi:10.1016/j.apsoil.2013.06.011

    Article  Google Scholar 

  • Eisenhauer N, Reich PB (2012) Above- and below-ground plant inputs both fuel soil food webs. Soil Biol Biochem 45:156–160. doi:10.1016/j.soilbio.2011.10.019

    Article  CAS  Google Scholar 

  • Feldman SR, Refi RO (2006) Cambios en la composición florística de un pastizal pampeano bajo diferentes prácticas de manejo. Cienc Investig Agrar 33:109–116

    Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression

  • Gange AC, Smith AK (2005) Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecol Entomol 30:600–606

    Article  Google Scholar 

  • Gange AC, Brown VK, Apllin DM (2003) Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol Lett 6:1051–1055. doi:10.1046/j.1461-0248.2003.00540.x

    Article  Google Scholar 

  • García Parisi PA, Casas C, Gundel PE, Omacini M (2012) Consequences of grazing on the vertical transmission of a fungal Neotyphodium symbiont in an annual grass population. Austral Ecol 37:620–628. doi:10.1111/j.1442-9993.2011.02325.x

    Article  Google Scholar 

  • Giordani CA (1973) Método para aprovechamiento de pasturas. Revista CREA 8:1–19

    Google Scholar 

  • Giufa M, Núñez JA (1992) Foraging by honeybees on Carduus acanthoides: pattern and efficiency. Ecol Entomol 17:326–330

    Article  Google Scholar 

  • Giufa M, Núñez JA (1993) Efficient floret inspection by honeybees in capitula of Carduus acanthoides. Ecol Entomol 18:116–122

    Article  Google Scholar 

  • Goulson D (1999) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect Plant Ecol Evol Syst 2:185–209

    Article  Google Scholar 

  • Gundel PE, Martínez-Ghersa MA, Garibaldi LA, Ghersa CM (2009) Viability of Neotyphodium endophytic fungus and endophyte-infected and noninfected Lolium multiflorum seeds. Botany 87:88–96. doi:10.1139/B08-119

    Article  Google Scholar 

  • Gundel PE, Pérez LI, Helander M, Saikkonen K (2013) Symbiotically modified organisms: nontoxic fungal endophytes in grasses. Trends Plant Sci 18:420–427. doi:10.1016/j.tplants.2013.03.003

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WE III, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402

    Article  Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342. doi:10.1146/annurev.ento.54.110807.090614

    Article  CAS  PubMed  Google Scholar 

  • Hol WHG, de Boer W, Termorshuizen AJ et al (2010) Reduction of rare soil microbes modifies plant- herbivore interactions. Ecol Lett 13:292–301. doi:10.1111/j.1461-0248.2009.01424.x

    Article  PubMed  Google Scholar 

  • Iannone LJ, Novas V, Young CA et al (2012) Endophytes of native grasses from South America: biodiversity and ecology. Fungal Ecol 5:357–363. doi:10.1016/j.funeco.2011.05.007

    Article  Google Scholar 

  • Joosten L, Mulder PPJ, Klinkhamer PGL, van Veen JA (2009) Soil-borne microorganisms and soil-type affect pyrrolizidine alkaloids in Jacobaea vulgaris. Plant Soil 325:133–143. doi:10.1007/s11104-009-9963-7

    Article  CAS  Google Scholar 

  • Kardol P, Cornips NJ, van Kempen MML et al (2007) Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162. doi:10.1890/06-0502

    Article  Google Scholar 

  • Koh S, Vicari M, Ball JP et al (2006) Rapid detection of fungal endophytes in grasses for large-scale studies. Funct Ecol 20:736–742. doi:10.1111/j.1365-2435.2006.01150.x

    Article  Google Scholar 

  • Kostenko O, van der Voorde TFJ, Mulder PPJ et al (2012) Legacy effects of aboveground-belowground interactions. Ecology 15:813–821. doi:10.1111/j.1461-0248.2012.01801.x

    Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166

    Article  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold S (2008) Plant – soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. doi:10.1111/j.1461-0248.2008.01209.x

    Article  PubMed  Google Scholar 

  • Lehtonen P, Helander M, Wink M et al (2005) Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol Lett 8:1256–1263. doi:10.1111/j.1461-0248.2005.00834.x

    Article  Google Scholar 

  • Leuchtmann A, Bacon CW, Schardl CL et al (2014) Nomenclatural realignment of Neotyphodium species with genus Epichloë. Mycologia 106:202–215. doi:10.3852/13-251

    Article  CAS  PubMed  Google Scholar 

  • Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940

    Article  CAS  Google Scholar 

  • Mandák B, Zákravský P, Kor D et al (2009) Low population differentiation and high genetic diversity in the invasive species Carduus acanthoides L. (Asteraceae) within its native range in the Czech Republic. Biol J Linn Soc 98:596–607

    Article  Google Scholar 

  • Matthews JW, Clay K, Feb N (2001) Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82:500–509

    Google Scholar 

  • Mikola J, Yeates GW, WARDLE DA et al (2001) Response of soil food-web structure to defoliation of different plant species combinations in an experimental grassaland community. Soil Biol Biochem 33:205–214

    Article  CAS  Google Scholar 

  • Mikola J, Nieminen M, Ilmarinen K, Vestberg M (2005) Belowground responses by AM fungi and animal trophic groups to repeated defoliation in an experimental grassland community. Soil Biol Biochem 37:1630–1639. doi:10.1016/j.soilbio.2005.01.027

    Article  CAS  Google Scholar 

  • Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601

    Article  Google Scholar 

  • Moore JC, Berlow EL, Coleman DC et al (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600. doi:10.1111/j.1461-0248.2004.00606.x

    Article  Google Scholar 

  • Novas VM, Iannone LJ, Godeas AM, Cabral D (2008) Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol Prog 8:75–81. doi:10.1007/s11557-008-0579-8

    Article  Google Scholar 

  • Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Syst 36:81–105. doi:10.1146/annurev.ecolsys.36.091704.175523

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81. doi:10.1038/35051070

    Article  CAS  PubMed  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Otero P (2004) Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos 104:581–590. doi:10.1111/j.0030-1299.2004.12915.x

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM (2005) A hierarchical framework for understanding the ecosystem consequences of endophyte-grass symbioses. In: Robert CA, West CP, Spiers DE (eds) Neothyphodium cool seas. Blackwell Publishing Ldt, Grasses, pp 141–162

    Google Scholar 

  • Omacini M, Eggers T, Bonkowski M et al (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232. doi:10.1111/j.1365-2435.2006.01099.x

    Article  Google Scholar 

  • Omacini M, Chaneton EJ, Bush L, Ghersa CM (2009) A fungal endosymbiont affects host plant recruitment through seed- and litter-mediated mechanisms. Funct Ecol 23:1148–1156. doi:10.1111/j.1365-2435.2009.01582.x

    Article  Google Scholar 

  • Pietikäinen A, Mikola J, Verstbers M, Setälä H (2009) Defoliation effects on Plantago lanceolata resource allocation and soil decomposers in relation to AM symbiosis and fertilization. Soil Biol Biochem 41:2328–2335

    Article  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS

  • Pinheiro J, Bates D, DebRoy S et al (2009) nlme: linear and nonlinear mixed effects models

  • Ponce MA, Bompadre MJ, Scervino JM et al (2009) Flavonoids, benzoic acids and cinnamic acids isolated from shoots and roots of Italian rye grass (Lolium multiflorum Lam.) with and without endophyte association and arbuscular mycorrhizal fungus. Biochem Syst Ecol 37:245–253. doi:10.1016/j.bse.2009.03.010

    Article  CAS  Google Scholar 

  • Reynolds HL, Packer A, Bever JD, Clay K (2008) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291

    Article  Google Scholar 

  • Rodríguez AM, Jacobo EJ (2010) Glyphosate effects on floristic composition and species diversity in the Flooding Pampa grassland (Argentina). Agric Ecosyst Environ 138:222–231. doi:10.1016/j.agee.2010.05.003

    Article  Google Scholar 

  • Rudgers JA, Orr S (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97:247–255. doi:10.1111/j.1365-2745.2008.01478.x

    Article  Google Scholar 

  • Rudgers JA, Holah J, Orr SP, Clay K (2007) Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 88:18–25

    Article  PubMed  Google Scholar 

  • Schardl CL, Young CA, Faulkner JR et al (2012) Chemotypic diversity of epichloae, fungal symbionts of grasses. Fungal Ecol 5:331–344. doi:10.1016/j.funeco.2011.04.005

    Article  Google Scholar 

  • Scherber C, Eisenhauer N, Weisser WW et al (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556. doi:10.1038/nature09492

    Article  CAS  PubMed  Google Scholar 

  • Schipper LA, Degens BP, Sparling GP, Duncan LC (2001) Changes in microbial heterotrophic diversity along five plant successional sequences. Soil Biol Biochem 33:2093–2103

    Article  CAS  Google Scholar 

  • Schon NL, Mackay AD, Yeates GW, Minor MA (2010) Separating the effects of defoliation and dairy cow treading pressure on the abundance and diversity of soil invertebrates in pastures. Appl Soil Ecol 46:209–221. doi:10.1016/j.apsoil.2010.08.011

    Article  Google Scholar 

  • Shafir S, Wiegmann DD, Smith BH, Real LA (1999) Risk-sensitive foraging: choice behaviour of honeybees in response to variability in volume of reward. Anim Behav 57:1055–1061

    Article  PubMed  Google Scholar 

  • Shiba T, Sugawara K, Arakawa A (2011) Evaluating the fungal endophyte Neotyphodium occultans for resistance to the rice leaf bug, Trigonotylus caelestialium, in Italian ryegrass, Lolium multiflorum. Entomol Exp Appl 141:45–51. doi:10.1111/j.1570-7458.2011.01162.x

    Article  CAS  Google Scholar 

  • Siegrist JA, McCulley RL, Bush LP, Phillips TD (2010) Alkaloids may not be responsible for endophyte-associated reductions in tall fescue decomposition rates. Funct Ecol 24:460–468. doi:10.1111/j.1365-2435.2009.01649.x

    Article  Google Scholar 

  • Sorensen LI, Mikola J, Kytöviita M (2008) Defoliation effects on plant and soil properties in an experimental low arctic grassland community – the role of plant community structure. Soil Biol Biochem 40:2596–2604. doi:10.1016/j.soilbio.2008.06.021

    Article  CAS  Google Scholar 

  • Sosa O, Martín B, Zerpa G, Montico S (2006) Evolución anual de la broza en diversas undidades forrajeras de un pastizal natural. Rev Cient Agropecu 10:33–45

    Google Scholar 

  • Striker GG, Insausti P, Grimoldi AA, Leon RJC (2006) Root strength and trampling tolerance in the grass Paspalum dilatatum and the dicot Lotus glaber in flooded soil. Funct Ecol 20:4–10. doi:10.1111/j.1365-2435.2006.01075.x

    Article  Google Scholar 

  • Suding KN, Harpole WS, Fukami T et al (2013) Consequences of plant – soil feedbacks in invasion. J Ecol 101:298–308. doi:10.1111/1365-2745.12057

    Article  Google Scholar 

  • Sugawara K, Inoue T, Yamashita M, Ohkubo H (2006) Distribution of the endophytic fungus, Neotyphodium occultans in naturalized Italian ryegrass in western Japan and its production of bioactive alkaloids known to repel insect pests. Grassl Sci 52:147–154. doi:10.1111/j.1744-697X.2006.00060.x

    Article  CAS  Google Scholar 

  • Tognetti PM, Chaneton EJ, Omacini M et al (2010) Exotic vs. native plant dominance over 20 years of old-field succession on set-aside farmland in Argentina. Biol Conserv 143:2494–2503. doi:10.1016/j.biocon.2010.06.016

    Article  Google Scholar 

  • Van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant – soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. doi:10.1111/1365-2745.12054

    Article  Google Scholar 

  • Veen GFC, De Vries S, Bakker ES et al (2014) Grazing-induced changes in plant – soil feedback alter plant biomass allocation. Oikos 123:800–806. doi:10.1111/j.1600-0706.2013.01077.x

    Article  Google Scholar 

  • Vignale MV, Iannone LJ, Scervino M, Novas MV (2014) Efecto de los exudados de endofitos Epichloë sobre el desarrollo in vitro de HMA. XIII Congr. Argentino Micol. Primera Reunion de la Asociación Micológica Carlos Spegazzini, Buenos Aires, Argentina, p 1

  • Walkley A, Black IA (1934) An examination of the digestion method for determining organic carbon in soils: effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–263

    Article  Google Scholar 

  • Wardle DA, Yeates GW, Williamson W, Bonner KI (2003) The response of a three trophic level soil food web to the identity and diversity of plant species and functional groups. Oikos 102:45–56

    Article  Google Scholar 

  • Wyatt R (1982) Inflorescence architecture: how flower number, arrangement, and phenology affect pollination and fruit-set. Am J Bot 585–594

Download references

Acknowledgments

We thank Till Eggers for his continued support of this work, Beatriz Santos for the English language edition and, María Semmartin and Luis Ignacio Perez for their comments on the manuscript. This study was financially supported by the grants from DAAD/SECYT DA0602 and CONICET-ANPCyT (PICT 2010) and, by the Ecology Department of Faculty of Agronomy, University of Buenos Aires. JPT and MO are affiliated to CONICET.

Author information

Authors and Affiliations

  1. Cátedra de Edafología, Universidad de Buenos Aires, Avenida San Martín 4453, Buenos Aires, CPA 1417 DSE, Argentina

    Cecilia Casas

  2. Cátedra de Botánica General, Universidad de Buenos Aires, Avenida San Martín 4453, Buenos Aires, CPA 1417 DSE, Argentina

    Juan Pablo Torretta

  3. IFEVA-CONICET, Cátedra de Ecología, Facultad de Agronomía, Universidad de Buenos Aires, Avenida San Martín 4453, Buenos Aires, CPA 1417 DSE, Argentina

    Marina Omacini

  4. Department of Biology/Chemistry, Division of Ecology, University of Osnabrueck, Barbarastr. 13, D-49076, Osnabrueck, Germany

    Nina Exeler

  5. CONICET, Buenos Aires, Argentina

    Juan Pablo Torretta

Authors
  1. Cecilia Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Pablo Torretta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nina Exeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marina Omacini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cecilia Casas.

Additional information

Responsible Editor: Andrea Campisano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 116 kb)

Fig S1

(GIF 30 kb)

High Resolution (TIFF 31047 kb)

Fig S2

(GIF 16 kb)

High Resolution (TIFF 18446 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Casas, C., Torretta, J.P., Exeler, N. et al. What happens next? Legacy effects induced by grazing and grass-endophyte symbiosis on thistle plants and their floral visitors. Plant Soil 405, 211–229 (2016). https://doi.org/10.1007/s11104-015-2644-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2644-9

Keywords

Search

Navigation