Cross-kingdom interactions matter: Fungal-mediated interactions structure an insect community on oak

Ecology Letters

Volumn 15, Issue 3, 2012, Pages 177-185

  Tack, Ayco J M ^a   Gripenberg, Sofia ^a,b   Roslin, Tomas ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

Erysiphe alphitoides; Indirect defence; Indirect interactions; Invasive species; Microsphaera alphitoides; Multi trophic interactions; Plant fungus insect interactions; Trait mediated interactions; Tripartite interactions

Indexed keywords

ARTHROPODA; ERYSIPHALES; ERYSIPHE ALPHITOIDES; FUNGI; HEXAPODA; QUERCUS ROBUR;

EID: 84931748985     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2011.01724.x     Document Type: Article

References (49)

1. Agrios, G.N. (2005). Plant Pathology, 5th edn. Academic press, New York, NY.
2. Biere, A., Elzinga, J.A., Honders, S.C. & Harvey, J.A. (2002). A plant pathogen reduces the enemy-free space of an insect herbivore on a shared host plant. Proc. R. Soc. Lond. B: Biol. Sci., 269, 2197-2204.
3. Bostock, R.M. (1999). Signal conflicts and synergies in induced resistance to multiple attackers. Physiol. Mol. Plant Pathol., 55, 99-109.
4. Braun, U. (1987). A monograph of the Erysiphales (powdery mildews). Beihefte zur Nova Hedwigia, 89, 1-700.
5. Cardoza, Y.J., Teal, P.E.A. & Tumlinson, J.H. (2003). Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environ. Entomol., 32, 970-976.
6. Crawley, M.J. (2007). The R Book. John Wiley and Sons Ltd, London.
7. Darwin, C. (1859). On the Origin of Species. John Murray, London, UK.
8. Desprez-Loustau, M.-L., Robin, C., Buée, M., Courtecuisse, R., Garbaye, J., Suffert, F. et al. (2007). The fungal dimension of biological invasions. Trends Ecol. Evol., 22, 472-480.
9. Edwards, M.C. & Ayres, P.G. (1982). Seasonal changes in resistance of Quercus petraea (sessile oak) leaves to Microsphaera alphitoides. Trans. Br. Mycol. Soc., 78, 569-571.
10. English-Loeb, G., Norton, A.P., Gadoury, D.M., Seem, R.C. & Wilcox, W.F. (1999). Control of powdery mildew in wild and cultivated grapes by a tydeid mite. Biol. Control, 14, 97-103.
11. Feeny, P. (1970). Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology, 51, 565-581.
12. Foëx, E. (1941). L'invasion des chênes d'Europe par le blanc ou oïdium. Revue des Eaux et Forêts, 79, 338-349.
13. Gause, G.F. (1934). The Struggle for Existence. Williams & Wilkins, Baltimore, MD.
14. Gripenberg, S., Morriën, E., Cudmore, A., Salminen, J.-P. & Roslin, T. (2007). Resource selection by female moths in a heterogeneous environment: what is a poor girl to do? J. Anim. Ecol., 76, 854-865.
15. Gripenberg, S., Ovaskainen, O., Morriën, E. & Roslin, T. (2008). Spatial population structure of a specialist leaf-mining moth. J. Anim. Ecol., 77, 757-767.
16. Hajji, M., Dreyer, E. & Marçais, B. (2009). Impact of Erysiphe alphitoides on transpiration and photosynthesis in Quercus robur leaves. Eur. J. Plant Pathol., 125, 63-72.
17. Hare, J.D. (2011). Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu. Rev. Entomol., 56, 161-180.
18. Hariot, M.P. (1907). Note sur un oidium du chêne. Bulletin de la Société Mycologique de France, 23, 157-159.
19. Hatcher, P.E. (1995). Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biological Reviews, 70, 639-694.
20. Hatcher, P.E., Paul, N.D., Ayres, P.G. & Whittaker, J.B. (1994). The effect of a foliar disease (rust) on the development of Gastrophysa viridula (Coleoptera: Chrysomelidae). Ecol. Entomol., 19, 349-360.
21. Honěk, A. (1993). Intraspecific variation in body size and fecundity in insects - a general relationship. Oikos, 66, 483-492.
22. Johnson, S.N., Douglas, A.E., Woodward, S. & Hartley, S.E. (2003). Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid. Oecologia, 134, 388-396.
23. Karban, R. & Baldwin, I.T. (1997). Induced Responses to Herbivory. University of Chicago Press, Chicago, IL.
24. Karban, R., Adamchak, R. & Schnathorst, W.C. (1987). Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science, 235, 678-680.
25. Kessler, A. & Baldwin, I.T. (2002). Plant responses to insect herbivory: the emerging molecular analysis. Ann. Rev. Plant Biol., 53, 299-328.
26. Kluth, S., Kruess, A. & Tscharntke, T. (2001). Interactions between the rust fungus Puccinia punctiformis and ectophagous and endophagous insects on creeping thistle. J. Appl. Ecol., 38, 548-556.
27. Laine, A.-L. (2004). A powdery mildew infection on a shared host plant affects the dynamics of the Glanville fritillary butterfly populations. Oikos, 107, 329-337.
28. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. & Schabenberger, O.. (2006). SAS® for Mixed Models, 2nd edn. SAS Institute Inc, Cary, NC.
29. Mondy, N. & Corio-Costet, M.-F. (2004). Feeding insects with a phytopathogenic fungus influences their diapause and population dynamics. Ecol. Entomol., 29, 711-717.
30. Moran, P. & Schultz, J.C. (1998). Ecological and chemical associations among late-season squash pests. Environ. Entomol., 27, 39-44.
31. Mougou, A., Dutech, C. & Desprez-Loustau, M.-L. (2008). New insights into the identity and origin of the causal agent of oak powdery mildew in Europe. Forest Pathol., 38, 275-287.
32. Mouttet, R., Bearez, P., Thomas, C. & Desneux, N. (2011). Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS ONE, 6, e18840.
33. Nimchuk, Z., Eulgem, T., Holt, B.F. III & Dangl, J.L. (2003). Recognition and response in the plant immune system. Annu. Rev. Genet., 37, 579-609.
34. van Nouhuys, S. & Laine, A.-L. (2008). Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly. Proc. R. Soc. B: Biol. Sci., 275, 787-795.
35. Omacini, M., Chaneton, E.J., Ghersa, C.M. & Müller, C.B. (2001). Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature, 409, 78-81.
36. Rasband, W.S. (19972011). ImageJ. U. S National Institutes of Health, Bethesda, MD. Last accessed 6 February 2011.
37. Röder, G., Rahier, M. & Naisbit, R.E. (2007). Coping with an antagonist: the impact of a phytopathogenic fungus on the development and behaviour of two species of alpine leaf beetle. Oikos, 116, 1514-1523.
38. Röder, G., Rahier, M. & Naisbit, R.E. (2011). Do induced responses mediate the ecological interactions between the specialist herbivores and phytopathogens of an alpine plant? PLoS ONE, 6, e19571.
39. Rostás, M., Simon, M. & Hilker, M. (2003). Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl. Ecol., 4, 43-62.
40. Simon, M. & Hilker, M. (2003). Herbivores and pathogens on willow: do they affect each other? Agric. For. Entomol., 5, 275-284.
41. Simon, M. & Hilker, M. (2005). Does rust infection of willow affect feeding and oviposition behavior of willow leaf beetles? J. Insect Behav., 18, 115-129.
42. Stout, M.J., Thaler, J.S. & Thomma, B.P.H.J. (2006). Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu. Rev. Entomol., 51, 663-689.
43. Strong, D.R., Lawton, J.H. & Southwood, T.R.E. (1984). Insects on Plants. Harvard University Press, Cambridge, USA.
44. Tack, A.J.M., Ovaskainen, O., Harrison, P.J. & Roslin, T. (2009). Competition as a structuring force in leaf miner communities. Oikos, 118, 809-818.
45. Tack, A.J.M., Ovaskainen, O., Pulkkinen, P. & Roslin, T. (2010). Spatial location dominates over host plant genotype in structuring an herbivore community. Ecology, 91, 2660-2672.
46. Tammaru, T., Kaitaniemi, P. & Ruohomaki, K. (1996). Realized fecundity in Epirrita autumnata (Lepidoptera: Geometridae): relation to body size and consequences to population dynamics. Oikos, 77, 407-416.
47. Taylor, J.E., Hatcher, P.E. & Paul, N.D. (2004). Crosstalk between plant responses to pathogens and herbivores: a view from the outside in. J. Exp. Bot., 55, 159-168.
48. Turlings, T.C.J. & Wäckers, F. (2003). Recruitment of predators and parasitoids by herbivore-injured plants. In: Advances in Insect Chemical Ecology (eds Cardé, R.T. & Millar, J.). Cambridge University Press, Cambridge, UK, pp. 21-75.
49. Yarwood, C.E. (1943). Association of thrips with powdery mildews. Mycologia, 35, 189-191.