Interactive effects of above- and belowground herbivory and plant competition on plant growth and defence

Basic and Applied Ecology

Volumn 16, Issue 6, 2015, Pages 500-509

  Jing, Jingying ^a   Raaijmakers, Ciska ^a   Kostenko, Olga ^a   Kos, Martine ^a   Mulder, Patrick P J ^b   Bezemer, T Martijn ^a  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Aboveground belowground interactions; Insect plant interactions; Leaf damage; Pyrrolizidine alkaloids; Root herbivory

Indexed keywords

EID: 84940794100     PISSN: 14391791     EISSN: 16180089     Source Type: Journal    
DOI: 10.1016/j.baae.2015.04.009     Document Type: Article

References (59)

1. Agrawal A.A. Resistance and susceptibility of milkweed: Competition, root herbivory, and plant genetic variation. Ecology 2004, 85:2118-2133.
2. Barbosa P., Hines J., Kaplan I., Martinson H., Szczepaniec A., Szendrei Z. Associational resistance and associational susceptibility: Having right or wrong neighbors. Annual Review of Ecology, Evolution and Systematics 2009, 40:1-20.
3. Barton K.E., Bowers M.D. Neighbor species differentially alter resistance phenotypes in Plantago. Oecologia 2006, 150:442-452.
4. 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.
5. Bezemer T.M., van Dam N.M. Linking aboveground and belowground interactions via induced plant defenses. Trends in Ecology and Evolution 2005, 20:617-624.
6. Bezemer T.M., Harvey J.A., Kowalchuk G.A., Korpershoek H., van der Putten W.H. Interplay between Senecio jacobaea and plant, soil, and aboveground insect community composition. Ecology 2006, 87:2002-2013.
7. Birdsall J., McCaughey W., Runyon J.B. Roads impact the distribution of noxious weeds more than restoration treatments in a lodgepole pine forest in Montana, U.S.A. Restoration Ecology 2011, 20:517-523.
8. Blossey B., Hunt-Joshi T.R. Belowground herbivory by insects: Influence on plants and aboveground herbivores. Annual Review of Entomology 2003, 48:521-547.
9. Carson W.P., Root R.B. Herbivory and plant species coexistence: Community regulation by an outbreaking phytophagous insect. Ecological Monographs 2000, 70:73-99.
10. Cheng D.D., Kirk H., Mulder P.P.J., Vrieling K., Klinkhamer P.G.L. Pyrrolizidine alkaloid variation in shoots and roots of segregating hybrids between Jacobaea vulgaris and Jacobaea aquatica. New Phytologist 2011, 192:1010-1023.
11. Clay K., Marks S., Cheplick G.P. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 1993, 74:1767-1777.
12. Clements D.R., Cole D.E., Darbyshire S., King J., McClay A. The biology of Canadian weeds. 128. Leucanthemum vulgare lam. Canadian Journal of Plant Science 2004, 84:343-363.
13. Crawley M.J. Plant-herbivore dynamics. Plant ecology 1997, 401-474. Blackwell Science, Oxford, UK. M.J. Crawley (Ed.).
14. Frischknecht P.M., Schuhmacher K., Müller-Schärer H., Baumann T.W. Phenotypic plasticity of Senecio vulgaris from contrasting habitat types: Growth and pyrrolizidine alkaloid formation. Journal of Chemical Ecology 2001, 27:343-358.
15. Graff P., Aguiar M.R., Chaneton E.J. Shift in positive and negative plant interactions along a grazing intensity gradient. Ecology 2007, 88:188-199.
16. Gurevitch J., Morrison J.A., Hedges L.V. The interaction between competition and predation: A meta-analysis of field experiments. American Naturalist 2000, 155:435-453.
17. Hambäck P.A., Beckerman A.P. Herbivory and plant resource competition: A review of two interacting interactions. Oikos 2003, 101:26-37.
18. Harper J.L., Wood W.A. Sencio jacobaea L. in biological flora of the British Isles. Journal of Ecology 1957, 45:617-637.
19. Hartmann T. Chemical ecology of pyrrolizidine alkaloids. Planta 1999, 207:483-495.
20. Hemerik L., Gort G., Brussaard L. Food preference of wireworms analyzed with multinomial Logit models. Journal of Insect Behavior 2003, 16:647-665.
21. Hol W.H.G., Macel M., van Veen J.A., van der Meijden E. Root damage and aboveground herbivory change concentration and composition of pyrrolizidine alkaloids of Senecio jacobaea. Basic and Applied Ecology 2004, 5:253-260.
22. Huang W., Carrillo J., Ding J.Q., Siemann E. Interactive effects of herbivory and competition intensity determine invasive plant performance. Oecologia 2012, 170:373-382.
23. Huang W., Carrillo J., Ding J.Q., Siemann E. Invader partitions ecological and evolutionary responses to above- and belowground herbivory. Ecology 2012, 93:2343-2352.
24. Hulme P.E. Herbivory, plant regeneration, and species coexistence. Journal of Ecology 1996, 84:609-615.
25. Ibanez S., Bison M., Lavorel S., Moretti M. Herbivore species identity mediates interspecific competition between plants. Community Ecology 2013, 14:41-47.
26. Johnson S.N., Clark K.E., Hartley S.E., Jones T.H., McKenzie S.W., Koricheva J. Aboveground-belowground herbivore interactions: A meta-analysis. Ecology 2012, 93:2208-2215.
27. Karban R., Baldwin I.T. Induced responses to herbivory 1997, The University of Chicago Press, Chicago, IL.
28. Kim T.N., Underwood N., Inouye B.D. Insect herbivores change the outcome of plant competition through both inter- and intraspecific processes. Ecology 2013, 94:1753-1763.
29. Kos M., Bukovinszky T., Mulder P.P.J., Bezemer T.M. Disentangling above- and belowground neighbor effects on the growth, chemistry and arthropod community on a focal plant. Ecology 2015, 96:164-175.
30. Kostenko O., Mulder P.P.J., Bezemer T.M. Effects of root herbivory on pyrrolizidine alkaloid content and aboveground plant-herbivore-parasitoid interactions in Jacobaea vulgaris. Journal of Chemical Ecology 2013, 39:109-119.
31. Kotowska A.M., Cahill J.F., Keddie B.A. Plant genetic diversity yields increased plant productivity and herbivore performance. Journal of Ecology 2010, 98:237-245.
32. Macel M., Bruinsma M., Dijkstra S.M., Ooijendijk T., Niemeyer H.M., Klinkhamer P.G.L. Differences in effects of pyrrolizidine alkaloids on five generalist insect herbivore species. Journal of Chemical Ecology 2005, 31:1493-1508.
33. Markham J., Chanway C. Measuring plant neighbor effects. Functional Ecology 1996, 10:548-549.
34. Maron J.L. Insect herbivory above- and belowground: Individual and joint effects on plant fitness. Ecology 1998, 79:1281-1293.
35. McEvoy P.B., Rudd N.T., Cox C.S., Huso M. Disturbance, competition, and herbivory effects on ragwort Senecio jacobaea populations. Ecological Monographs 1993, 63:55-75.
36. McNutt D.W., Halpern S.L., Barrows K., Underwood N. Intraspecific competition facilitates the evolution of tolerance to insect damage in the perennial plant Solanum carolinense. Oecologia 2012, 170:1033-1044.
37. Mraja A., Unsicker S., Reichelt M., Gershenzon J., Roscher C. Plant community diversity influences allocation to direct chemical defense in Plantago lanceolata. PLoS ONE 2011, 6:e28055.
38. Müller-Schärer H., Brown V.K. Direct and indirect effects of aboveground and belowground insect herbivory on plant-density and performance of Tripleurospermum perforatum during early plant succession. Oikos 1995, 72:36-41.
39. Pearson A.C. Biology, population dynamics, and pest status of the beet armyworm (Spodoptera exigua) in the imperial valley of California 1982, University of California, Riverside, CA, USA, (PhD dissertation).
40. Price P.W. The plant vigor hypothesis and herbivore attack. Oikos 1991, 62:244-251.
41. R Core Team R: A language and environment for statistical computing 2014, R Foundation for Statistical Computing, Vienna, Austria, 〈http://www.r-project.org/〉.
42. Ramsell J., Malloch A.J.C., Whittaker J. When grazed by Tipula paludosa, Lolium perenne is a stronger competitior of Rumex obtusifolius. Journal of Ecology 1993, 81:777-786.
43. Rees M., Brown V.K. Interactions between invertebrate herbivores and plant competition. Journal of Ecology 1992, 80:353-360.
44. Sagareishvili T.G. Alkaloids of Leucanthemum vulgare. Chemistry of Natural Compounds 2000, 36:327.
45. Schädler M., Brandl R., Haase J. Antagonistic interactions between plant competition and insect herbivory. Ecology 2007, 88:1490-1498.
46. Siemens D.H., Garner S.H., Mitchell-Olds T., Callaway R.M. Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 2002, 83:505-517.
47. Singh P., Unnithan G.C., Delobel A.G.L. An artificial diet for sorghum shootfly larvae. Entomologia Experimentalis et Applicata 1983, 33:122-124.
48. Soler R., van der Putten W.H., Harvey J.A., Vet L.E.M., Dicke M., Bezemer T.M. Root herbivore effects on aboveground multitrophic interactions: Patterns, processes and mechanisms. Journal of Chemical Ecology 2012, 38:755-767.
49. Suwa T., Louda S.M. Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle. Oecologia 2012, 169:467-476.
50. Tahvanainen J.O., Root R.B. The influence of vegetational diversity on the population ecology of a specialised herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 1972, 10:321-346.
51. Underwood N., Inouye B.D., Hambäck P.A. A conceptual framework for associational effects: When do neighbors matter and how would we know?. The Quarterly Review of Biology 2014, 89:1-19.
52. van Dam N.M. Belowground herbivory and plant defenses. Annual Review of Ecology, Evolution and Systematics 2009, 40:373-391.
53. van de Voorde T.F.J., van der Putten W.H., Bezemer T.M. Intra- and interspecific plant-soil interactions, soil legacies and priority effects during old-field succession. Journal of Ecology 2011, 99:945-953.
54. van der Meijden R. Heukels' Flora van Nederland 1990, Wolters-Noordhoff, Groningen, The Netherlands.
55. van Ruijven J., De Deyn G.B., Raaijmakers C.E., Berendse F., van der Putten W.H. Interactions between spatially separated herbivores indirectly alter plant diversity. Ecology Letters 2005, 8:30-37.
56. Wardle D.A., Barker G.M. Competition and herbivory in establishing grassland communities: Implications for plant biomass, species diversity and soil microbial activity. Oikos 1997, 80:470-480.
57. Wardle D.A., Bardgett R.D., Klironomos J.N., Setala H., van der Putten W.H., Wall D.H. Ecological linkages between aboveground and belowground biota. Science 2004, 304:1629-1633.
58. Weber E. Invasive plant species of the world: A reference guide to environmental weeds 2003, CABI Publishing, UK.
59. Weigelt A., Jolliffe P. Indices of plant competition. Journal of Ecology 2003, 91:707-720.