Skip to main content
SpringerLink
Log in

Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata

  • Community Ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

In this study we tested for trade-offs between the benefit arbuscular mycorrhizal (AM) fungi provide for hosts and their competitive ability in host roots, and whether this potential trade-off shifts in the presence of a plant stress (herbivory). We used three species of AM fungi previously determined to vary in host growth promotion and spore production in association with host plants. We found that these AM fungal species competed for root space, and the best competitor, Scutellospora calospora, was the worst mutualist. In addition, the worst competitor, Glomus white, was the best mutualist. Competition proved to have stronger effects on fungal infection patterns than herbivory, and competitive dominance was not altered by herbivory. We found a similar pattern in a previous test of competition among AM fungi, and we discuss the implications of these results for the persistence of the mutualism and feedbacks between AM fungi and their plant hosts.

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

Similar content being viewed by others

References

  • Abbott LK (1982) Comparative anatomy of vesicular arbuscular mycorrhizas formed on subterranean clover. Aust J Bot 30:485–499

    Article  Google Scholar 

  • Bennett AE, Bever JD (2007) Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88:210–218

    Article  PubMed  Google Scholar 

  • Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia (in press)

  • Bever JD (2002a) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond B Biol Sci 269:2595–2601

    Article  Google Scholar 

  • Bever JD (2002b) Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290

    Article  CAS  Google Scholar 

  • Bever JD, Schultz PA, Pringle A, Morton JB (2001) Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. Bioscience 51:923–931

    Article  Google Scholar 

  • Bobbitt JM, Segebarth KP (1969) Iridoid glycosides and similar substances. In: Taylor WI, Battersby AR (eds) Cyclopentanoid terpene derivatives. Dekker, New York, pp 1–145

    Google Scholar 

  • Bowers MD, Collinge SK (1992) Fate of iridoid glycosides in different life stages of the buckeye, Junonia coenia (Lepidoptera, Nymphalidae). J Chem Ecol 18:817–831

    Article  CAS  Google Scholar 

  • Bowers MD, Puttick GM (1986) Fate of ingested iridoid glycosides in Lepidopteran herbivores. J Chem Ecol 12:169–178

    Article  CAS  Google Scholar 

  • Bronstein JL, Wilson WG, Morris WE (2003) Ecological dynamics of mutualist/antagonist communities. Am Nat 162:S24–S39

    Article  PubMed  Google Scholar 

  • Cano C, Bago A (2005) Competition and substrate colonization strategies of three polyxenically grown arbuscular mycorrhizal fungi. Mycologia 97:1201–1214

    Article  PubMed  Google Scholar 

  • Currie AF, Murray PJ, Gange AC (2006) Root herbivory by Tipula paludosa larvae increases colonization of Agrostis capillaris by arbuscular mycorrhizal fungi. Soil Biol Biochem 38:1994–1997

    Article  CAS  Google Scholar 

  • Duff RB, Bacon JSD, Mundie CM, Farmer VC, Russell JD, Forrester AR (1965) Catalpol and methylcatalpol—naturally occurring glycosides in Plantago and Buddleia species. Biochem J 96:1–7

    PubMed  CAS  Google Scholar 

  • Fineblum WL, Rausher MD (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517–520

    Article  CAS  Google Scholar 

  • Gange AC (2007) Insect–mycorrhizal interactions: patterns, processes, and consequences. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, London, pp 124–143

    Google Scholar 

  • Gange AC, Bower E, Brown VK (2002) Differential effects of insect herbivory on arbuscular mycorrhizal colonization. Oecologia 131:103–112

    Article  Google Scholar 

  • Gange AC, Brown VK, Aplin DM (2005) Ecological specificity of arbuscular mycorrhzae: evidence from foliar- and seed-feeding insects. Ecology 86:603–611

    Article  Google Scholar 

  • Gehring CA, Whitham TG (1994) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9:251–255

    Article  Google Scholar 

  • Gehring CA, Whitham TG (2002) Mycorrhizae–herbivore interactions: population and community consequences. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology, vol 157. Springer, Berlin, pp 295–320

    Google Scholar 

  • Gloer JB (1995) The chemistry of fungal antagonism and defense. Can J Bot 73:S1265–S1274

    Article  CAS  Google Scholar 

  • Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344

    Article  Google Scholar 

  • Hart MM, Reader RJ (2005) The role of the external mycelium in early colonization for three arbuscular mycorrhizal fungal species with different colonization strategies. Pedobiologia 49:269–279

    Article  Google Scholar 

  • Hepper CM, Azconaguilar C, Rosendahl S, Sen R (1988) Competition between 3 species of Glomus used as spatially separated introduced and indigenous mycorrhizal inocula for leek (Allium porrum L). New Phytol 110:207–215

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The Dilemma of plants—to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hoeksema JD, Kummel M (2003) Ecological persistence of the plant–mycorrhizal mutualism: a hypothesis from species coexistence theory. Am Nat 162:S40–S50

    Article  PubMed  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–586

    Article  Google Scholar 

  • Kennedy PG, Hortal S, Bergemann SE, Bruns TD (2007) Competitive interactions among three ectomycorrhizal fungi and their relation to host plant performance. J Ecol 95:1338–1345

    Article  CAS  Google Scholar 

  • Kiers ET, van der Heijden MGA (2006) Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87:1627–1636

    Article  PubMed  Google Scholar 

  • Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–S62

    Article  PubMed  Google Scholar 

  • Kula AAR, Hartnett DC, Wilson GWT (2005) Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions. Ecol Lett 8:61–69

    Article  Google Scholar 

  • Merryweather J, Fitter A (1998) The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta. I. Diversity of fungal taxa. New Phytol 138:117–129

    Article  Google Scholar 

  • Miller TEX (2007) Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 116:500–512

    Article  Google Scholar 

  • Mueller RC, Sthultz CM, Martinez T, Gehring CA, Whitham TG (2005) The relationship between stem-galling wasps and mycorrhizal colonization of Quercus turbinella. Can J Bot 83:1349–1353

    Article  Google Scholar 

  • Palmer TM, Stanton ML, Young TP (2003) Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am Nat 162:S63–S79

    Article  PubMed  Google Scholar 

  • Pearson JN, Abbott LK, Jasper DA (1993) Mediation of competition between 2 colonizing va mycorrhizal fungi by the host plant. New Phytol 123:93–98

    Article  Google Scholar 

  • Pearson JN, Abbott LK, Jasper DA (1994) Phosphorus, soluble carbohydrates and the competition between 2 arbuscular mycorrhizal fungi colonizing subterranean clover. New Phytol 127:101–106

    Article  CAS  Google Scholar 

  • Sen R, Hepper CM, Azconaguilar C, Rosendahl S (1990) Competition between introduced and indigenous mycorrhizal fungi (Glomus spp) for root colonization of leek. Agric Ecosyst Environ 29:355–359

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London

    Google Scholar 

  • Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23

    Article  PubMed  Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Strauss SY, Conner JK, Lehtila KP (2001) Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness. Am Nat 158:496–504

    Article  PubMed  CAS  Google Scholar 

  • Thrall PH, Burdon JJ (2003) Evolution of virulence in a plant host–pathogen metapopulation. Science 299:1735–1737

    Article  PubMed  CAS  Google Scholar 

  • Wamberg C, Christensen S, Jakobsen I (2003) Interaction between foliar-feeding insects, mycorrhizal fungi, and rhizosphere Protozoa on pea plants. Pedobiologia 47:281–287

    Article  Google Scholar 

  • Wilson JM (1984) Competition for infection between vesicular arbuscular mycorrhizal fungi. New Phytol 97:427–435

    Article  Google Scholar 

  • Wilson JM, Trinick MJ (1983) Infection development and interactions between vesicular–arbuscular mycorrhizal fungi. New Phytol 93:543–553

    Article  Google Scholar 

  • Yu DW, Pierce NE (1998) A castration parasite of an ant–plant mutualism. Proc R Soc Lond B Biol Sci 265:375–382

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank David McNutt, Julie Gummow, Dacia Montemayor, Alex Nguyen, Tommy Zajac, and Deane Bowers for assistance with data collection, protocols, and equipment; and Fred Nijhout, Laura Grunert, and Deane Bowers for providing J. coenia butterflies, and help rearing them. We would like to thank Keith Clay, Heather Reynolds, Curt Lively, Peggy Schultz, Scott Mangan, Tom Platt, Jennifer Rudgers, Jon Haloin, Michael Dawson, Mirka Macel, Pat McIntyre, Elizabeth Seifer, and the Bever/Schultz lab group for taking the time to review and discuss this paper with us. We would like to thank Jason Hoeksema, Peter Kennedy, and two anonymous reviewers for their comments on the manuscript. We acknowledge the support of Sigma Xi Grant-In-Aid of Research, Indiana University McCormick Grant, and NSF grants DEB-0407816 to Alison Bennett and DEB-0049080 to Jim Bever. All experiments comply with the current laws of the United States.

Author information

Author notes

  1. Alison Elizabeth Bennett

    Present address: University of Wisconsin, 237 Russell Labs, 1630 Linden Drive, Madison, WI, 53706-1598, USA

Authors and Affiliations

  1. Indiana University, 1001 E. 3rd Street, Bloomington, IN, 47405, USA

    Alison Elizabeth Bennett & James D. Bever

Authors
  1. Alison Elizabeth Bennett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James D. Bever
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alison Elizabeth Bennett.

Additional information

Communicated by Jeremy Burdon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bennett, A.E., Bever, J.D. Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata . Oecologia 160, 807–816 (2009). https://doi.org/10.1007/s00442-009-1345-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1345-6

Keywords

Search

Navigation