Download PDF
Plant Biol (Stuttg) 2004; 6(2): 231-238
DOI: 10.1055/s-2004-817846
Original Paper

Georg Thieme Verlag Stuttgart · New York

Above- and Belowground Trophic Interactions on Creeping Thistle (Cirsium arvense) in High- and Low-Diversity Plant Communities: Potential for Biotic Resistance?

T. M. Bezemer1 , O. Graça2 , P. Rousseau2 , W. H. van der Putten1 , 2
  • 1Netherlands Institute of Ecology (NIOO-KNAW), Centre for Terrestrial Ecology, Heteren, The Netherlands
  • 2Laboratory of Nematology, Wageningen University, PO Box 8123, 6700 ES Wageningen, The Netherlands
Further Information

Publication History

Publication Date:
26 March 2004 (online)

   Permissions and Reprints

Abstract

The capacity of local communities to control introduced plants is called biotic resistance. Biotic resistance has been almost exclusively tested for plant competition and aboveground herbivores and pathogens, while neglecting root herbivores and soil pathogens. Here, we present biotic resistance by above- and belowground herbivores in concert, and relate the abundance of the plant enemies to the species diversity of the local plant communities. The study was carried out in a 7-year-old biodiversity field experiment. We used creeping thistle (Cirsium arvense) as a model, and quantified sap-sucking herbivores: aboveground aphids, their antagonists, and root-feeding nematodes. As plant diversity treatments, we used field plots sown with high (15 plant species, HSD) or low (4 plant species, LSD) diverse seed mixtures in 1996 and that were not weeded. Creeping thistle became established spontaneously at the start of the experiment. In 2002, in HSD plots, 90 % of the plant community was made up by 11 species, compared to seven species in LSD plots. No differences were found for C. arvense abundance or biomass. Aboveground, three aphid species were found on C. arvense-Uroleucon cirsii, Aphis fabae, and Macrosiphum euphorbiae, but the latter was found only in low densities. Significantly more aphid species were found on individual plants in HSD plots. Moreover, in HSD plots, on average 10 % of aphids were parasitized, while no parasitism was observed in LSD plots. In the root zone of C. arvense, significantly more nematodes were found in HSD than in LSD plots, and a significantly higher proportion of those nematodes were plant parasites. The dominant plant parasitic nematode in both treatments was Paratylenchus. We conclude that biotic resistance by natural enemies may be enhanced by plant species diversity, but that above- and belowground sap-sucking herbivores do not necessarily have to respond similarly to the diversity of the surrounding plant community.

Key words

Aphis fabae - Macrosiphum euphorbiae - nematode - Paratylenchus - Uroleucon cirsii.

References

  • 1 Bardgett R. D., Cook R.. Functional aspects of soil animal diversity in agricultural grasslands.  Applied Soil Ecology. (1998);  10 263-276
    CrossrefPubMedGoogle Scholar
  • 2 Bardgett R. D., Wardle D. A., and Yeates G. W.. Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms.  Soil Biology and Biochemistry. (1998);  30 1867-1878
    CrossrefPubMedGoogle Scholar
  • 3 Bezemer T. M., Wagenaar R., Van Dam N. M., Wäckers F. L.. Interactions between above- and belowground insect herbivores as mediated by the plant defense system.  Oikos. (2003);  101 555-562
    CrossrefPubMedGoogle Scholar
  • 4 Bezemer T. M., Wagenaar R., Van Dam N. M., Van der Putten W. H., Wäckers F. L.. Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury.  Journal of Chemical Ecology. (2004);  30 53-67
    CrossrefPubMedGoogle Scholar
  • 5 Bongers T.. De Nematoden van Nederland. Pirola Schoorl, The Netherlands (1988)
    Google Scholar
  • 6 Brown V. K., Gange A. C.. Insect herbivory below ground.  Advances in Ecological Research. (1990);  20 1-58
    PubMedGoogle Scholar
  • 7 Burrows R. L., Pfleger F. L.. Arbuscular mycorrhizal fungi respond to increasing plant diversity.  Canadian Jounal of Botany. (2002);  80 120-130
    PubMedGoogle Scholar
  • 8 Davis M. A., Grime J. P., Thompson K.. Fluctuating resources in plant communities: a general theory of invasibility.  Journal of Ecology. (2000);  88 528-534
    CrossrefPubMedGoogle Scholar
  • 9 De Deyn G. B., Raaijmakers C. E., Zoomer R. H., Berg M. P., De Ruiter P. C., Verhoef H. A., Bezemer T. M., Van der Putten W. H.. Soil invertebrate fauna enhances grassland succession and diversity.  Nature. (2003);  422 711-713
    CrossrefPubMedGoogle Scholar
  • 10 Edwards G. R., Bourdot G. W., Crawley M. J.. Influence of herbivory, competition and soil fertility on the abundance of Cirsium arvense in acid grassland.  Journal of Applied Ecology. (2000);  37 321-334
    CrossrefPubMedGoogle Scholar
  • 11 Elton C. S.. The Ecology of Invasions by Animals and Plants. London, UK; Methuen and Co. (1958)
    Google Scholar
  • 12 Gange A. C.. Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant.  New Phytologist. (2001);  150 611-618
    CrossrefPubMedGoogle Scholar
  • 13 Gange A. C., Brown V. K.. Effects of root herbivory by an insect on a foliar-feeding species, mediated through changes in the host plant.  Oecologia. (1989);  81 38-42
    CrossrefPubMedGoogle Scholar
  • 14 Haddad N. M., Tilman D., Haarstad J., Ritchie M., Knops J. M. H.. Contrasting effects of plant richness and composition on insect communities: A field experiment.  American Naturalist. (2001);  158 17-35
    PubMedGoogle Scholar
  • 15 Harris P., Shorthouse J. D.. Effectiveness of gall inducers in weed biological control.  Canadian Entomologist. (1996);  128 1021-1055
    PubMedGoogle Scholar
  • 16 Hector A., Schmid B., Beierkuhnlein C., Caldeira M. C., Diemer M., Dimitrakopoulos P. G., Finn J. A., Freitas H., Giller P. S., Good J., Harris R., Hogberg P., Huss-Danell K., Joshi J., Jumpponen A., Körner C., Leadley P. W., Loreau M., Minns A., Mulder C. P. H., O'Donovan G., Otway S. J., Pereira J. S., Prinz A., Read D. J., Scherer-Lorenzen M., Schulze E. D., Siamantziouras A. S. D., Spehn E. M., Terry A. C., Troumbis A. Y., Woodward F. I., Yachi S., Lawton J. H.. Plant diversity and productivity experiments in European grasslands.  Science. (1999);  286 1123-1127
    CrossrefPubMedGoogle Scholar
  • 17 Hooper D. U., Bignell D. E., Brown V. K., Brussaard L., Dangerfield J. M., Wall D. H., Wardle D. A., Coleman D. C., Giller K. E., Lavelle P., Van der Putten W. H., De Ruiter P. C., Rusek J., Silver W. L., Tiedje J. M., Wolters V.. Interactions between above-ground and below-ground biodiversity in terrestrial ecosystems: Patterns, mechanisms, and feedbacks.  Bioscience. (2000);  50 1049-1061
    PubMedGoogle Scholar
  • 18 Jervis M. A., Kidd N. A. C., Fitton M. G., Huddleston T., Dawah H. A.. Flower-visiting by hymenopteran parasitoids.  Journal of Natural History. (1993);  27 67-105
    PubMedGoogle Scholar
  • 19 Knops J. M. H., Tilman D., Haddad N. M., Naeem S., Mitchell C. E., Haarstad J., Ritchie M. E., Howe K. M., Reich P. B., Siemann E., Groth J.. Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity.  Ecology Letters. (1999);  2 286-293
    CrossrefPubMedGoogle Scholar
  • 20 Kluth S., Kruess A., Tscharntke T.. Insects as vectors of plant pathogens: mutualistic and antagonistic interactions.  Oecologia. (2002);  133 193-199
    CrossrefPubMedGoogle Scholar
  • 21 Koricheva J., Mulder C. P. H., Schmid B., Joshi J., Huss-Danell K.. Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands.  Oecologia. (2000);  125 271-282
    CrossrefPubMedGoogle Scholar
  • 22 Korthals G. W., Smilauer P., van Dijk C., Van der Putten W. H.. Linking above- and below-ground biodiversity: abundance and trophic complexity in soil as a response to experimental plant communities on abandoned arable land.  Functional Ecology. (2001);  15 506-514
    CrossrefPubMedGoogle Scholar
  • 23 Lepš J., Brown V. K., Len T. A. D., Gormsen D., Hedlund K., Kailova J.,  Korthals G. W., Mortimer S. R., Rodriguez-Barrueco C., Roy J., Regina I. S., van Dijk C., Van der Putten W. H.. Separating the chance effect from other diversity effects in the functioning of plant communities.  Oikos. (2001);  92 123-134
    CrossrefPubMedGoogle Scholar
  • 24 Malý S., Korthals G. W., Van Dijk C., Van der Putten W. H., De Boer W.. Effect of vegetation manipulation of abandoned arable land on soil microbial properties.  Biology and Fertility of Soils. (2000);  31 121-127
    CrossrefPubMedGoogle Scholar
  • 25 Maron J. L., Vila M.. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses.  Oikos. (2001);  95 361-373
    CrossrefPubMedGoogle Scholar
  • 26 Masters G. J.. The impact of root herbivory on aphid performance: Field and laboratory evidence.  Acta Oecologica. (1995);  16 135-142
    PubMedGoogle Scholar
  • 27 Masters G. J., Brown V. K.. Plant-mediated interactions between two spatially separated insects.  Functional Ecology. (1992);  6 175-179
    PubMedGoogle Scholar
  • 28 Masters G. J., Brown V. K., Gange A. C.. Plant mediated interactions between above- and below-ground insect herbivores.  Oikos. (1993);  66 148-151
    PubMedGoogle Scholar
  • 29 Masters G. J., Jones T. H., Rogers M.. Host-plant mediated effects of root herbivory on insect seed predators and their parasitoids.  Oecologia. (2001);  127 246-250
    CrossrefPubMedGoogle Scholar
  • 30 May R. M.. How many species?.  Philosophical Transactions of the Royal Society of London B. (1990);  327 171-182
    PubMedGoogle Scholar
  • 31 Mitchell C. E., Power A. G.. Release of invasive plants from fungal and viral pathogens.  Nature. (2003);  421 625-627
    CrossrefPubMedGoogle Scholar
  • 32 Moran N. A., Whitham T. G.. Interspecific competition between root-feeding and leaf-galling aphids mediated by host-plant resistance.  Ecology. (1990);  71 1050-1058
    PubMedGoogle Scholar
  • 33 Mortimer S. R., Booth R. G., Harris S. J., Brown V. K.. Effects of initial site management on the Coleoptera assemblages colonising newly established chalk grassland on ex-arable land.  Biological Conservation. (2002);  104 301-313
    CrossrefPubMedGoogle Scholar
  • 34 Mulder C. P. H., Koricheva J., Huss-Danell K., Hogberg P., Joshi J.. Insects affect relationships between plant species richness and ecosystem processes.  Ecology Letters. (1999);  53 819-829
    PubMedGoogle Scholar
  • 35 Novozamsky I., Houba V. J. G., Temminghof E., Van der Lee J. J.. Determination of “total” N and “total” P in a single soil digest.  Netherlands Journal of Agricultural Science. (1984);  32 322-324
    PubMedGoogle Scholar
  • 36 Oostenbrink M.. Estimating nematode populations by some selected methods. Sasser, J. N. and Jenkins, W. R., eds. Nematology. Chapel Hill, NC; University of North Carolina Press (1960): 85-102
    Google Scholar
  • 37 Root R. B.. Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleraceae). .  Ecological Monographs. (1973);  43 95-124
    PubMedGoogle Scholar
  • 38 Salt D. T., Fenwick P., Whittaker J. B.. Interspecific herbivore interactions in a high CO2 environment: Root and shoot aphids feeding on Cardamine. .  Oikos. (1996);  77 326-330
    PubMedGoogle Scholar
  • 39 Siemann E., Tilman D., Haarstad J., Ritchie M.. Experimental tests of the dependence of arthropod diversity on plant diversity.  American Naturalist. (1998);  152 738-750
    CrossrefPubMedGoogle Scholar
  • 40 Southwood T. R. E., Brown V. K., Reader P. M.. The relationships of plant and insect diversities in succession.  Biological Journal of the Linnean Society. (1979);  12 327-348
    PubMedGoogle Scholar
  • 41 Spehn E. M., Joshi J., Schmid B., Alpei J., Korner C.. Plant diversity on soil heterotrophic activity in experimental grassland systems.  Plant and Soil. (2000);  224 217-230
    CrossrefPubMedGoogle Scholar
  • 42 Stanton N. L.. The underground in grasslands.  Annual Review of Ecology and Systematics. (1988);  19 573-589
    CrossrefPubMedGoogle Scholar
  • 43 Stephan A., Meyer A. H., Schmid B.. Plant diversity affects culturable soil bacteria in experimental grassland communities.  Journal of Ecology. (2000);  88 988-998
    CrossrefPubMedGoogle Scholar
  • 44 Tilman D., Wedin D., Knops J.. Productivity and sustainability influenced by biodiversity in grassland ecosystems.  Nature. (1996);  379 718-720
    CrossrefPubMedGoogle Scholar
  • 45 Van Dam N. M., Harvey J. A., Wäckers F. L., Bezemer T. M., Van der Putten W. H., Vet L. E. M.. Interactions between aboveground and belowground induced responses against phytophages.  Basic and Applied Ecology. (2003);  4 63-77
    PubMedGoogle Scholar
  • 46 Van der Putten W. H., Mortimer S. R., Hedlund K., Van Dijk C., Brown V. K., Lěps J., Rodriguez-Barrueco C., Roy J., Len T. A. D., Gormsen D., Korthals G. W., Lavorel S., Regina I. S., Smilauer P.. Plant species diversity as a driver of early succession in abandoned fields: a multi-site approach.  Oecologia. (2000);  124 91-99
    CrossrefPubMedGoogle Scholar
  • 47 Van der Putten W. H., Vet L. E. M., Harvey J. A., Wackers F. L.. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists.  Trends in Ecology and Evolution. (2001);  16 547-554
    CrossrefPubMedGoogle Scholar
  • 48 Wardle D. A., Van der Putten W. H.. Biodiversity, ecosystem functioning and above-ground-below-ground linkages. Loreau, M., Naeem, S., and Inchausti, P., eds. Biodiversity and Ecosystem Functioning: Synthesis and Perspectives. Oxford, UK; Oxford University Press (2002): 155-168
    Google Scholar
  • 49 Wardle D. A., Bonner K. I., Barker G. M., Yeates G. W., Nicholson K. S., Bardgett R. D., Watson R. N., Ghani A.. Plant removals in perennial grassland: Vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties.  Ecological Monographs. (1999);  69 535-568
    PubMedGoogle Scholar
  • 50 Yeates G. W., Wardle D. A., Watson R. N.. Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period.  Soil Biology and Biochemistry. (1999);  31 1721-1733
    CrossrefPubMedGoogle Scholar

T. M. Bezemer

Netherlands Institute of Ecology
Centre for Terrestrial Ecology

P.O. Box 40

6666 ZG Heteren

The Netherlands

Email: m.bezemer@nioo.knaw.nl

Section Editor: M. C. Ball

      >