Trophic cascades initiated by fungal plant endosymbionts impair reproductive performance of parasitoids in the second generation

Oecologia

Volumn 157, Issue 3, 2008, Pages 399-407

  Härri, Simone A ^a,c   Krauss, Jochen ^a,b   Müller, Christine B ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF BAYREUTH   (Germany)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

Bottom up cascades; Endophyte; Indirect effects; Multi trophic interactions; Neotyphodium lolii

Indexed keywords

APHID; ENDOPHYTE; ENDOSYMBIONT; FUNGUS; GRASS; HERBIVORE; HOST QUALITY; PARASITISM; PARASITOID; REPRODUCTION; TOXIN; TROPHIC CASCADE; TROPHIC INTERACTION;

ANIMAL; APHID; ARTICLE; FEMALE; FOOD CHAIN; FUNGUS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; LOLIUM; MALE; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; REPRODUCTION; SYMBIOSIS; WASP;

ANIMALS; APHIDS; FEMALE; FOOD CHAIN; FUNGI; HOST-PARASITE INTERACTIONS; LOLIUM; MALE; REPRODUCTION; SYMBIOSIS; WASPS;

APHIDIDAE; APHIDIUS ERVI; LOLIUM PERENNE; METOPOLOPHIUM FESTUCAE; NEOTYPHODIUM LOLII; POACEAE;

EID: 49249137029     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-008-1094-y     Document Type: Article

References (47)

1. PA Abrams 1995 Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities Am Nat 146 112 134
2. P Barbosa P Gross J Kemper 1991 Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata Ecology 72 1567 1575
3. GM Barker PJ Addison 1996 Influence of clavicipitaceous endophyte infection in ryegrass on development of the parasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae) in Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae) Biol Control 7 281 287
4. TL Bultman KL Borowicz RM Schneble TA Coudron LP Bush 1997 Effect of a fungal endophyte on the growth and survival of two Euplectrus parasitoids Oikos 78 170 176
5. TL Bultman MR McNeill SL Goldson 2003 Isolate-dependent impacts of fungal endophytes in a multitrophic interaction Oikos 102 491 496
6. LP Bush HH Wilkinson CL Schardl 1997 Bioprotective alkaloids of grass-fungal endophyte symbioses Plant Physiol 114 1 7
7. BC Campbell SS Duffey 1979 Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control Science 205 700 702
8. SR Carpenter JF Kitchell JR Hodgson 1985 Cascading trophic interactions and lake productivity Bioscience 35 634 639
9. K Clay 1990 Fungal endophytes of grasses Annu Rev Ecol Syst 21 275 297
10. RF Denno C Gratton MA Peterson GA Langellotto DL Finke AF Huberty 2002 Bottom-up forces mediate natural-enemy impact in a phytophagous insect community Ecology 83 1443 1458
11. Dixon AFG (1998) Aphid ecology, 2nd edn. Chapman & Hall, London
12. Faeth SH, Bultman TL (2002) Endophytic fungi and interactions among host plants, herbivores and natural enemies. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 89-123
13. LK Finkes AB Cady JC Mulroy K Clay JA Rudgers 2006 Plant-fungus mutualism affects spider composition in successional fields Ecol Lett 9 347 356
14. F Francis G Lognay JP Wathelet E Haubruge 2001 Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata J Chem Ecol 27 243 256
15. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton
16. SL Goldson JR Proffitt LR Fletcher DB Baird 2000 Multitrophic interaction between the ryegrass Lolium perenne, its endophyte Neotyphodium lolii, the weevil pest Listronotus bonariensis, and its parasitoid Microctonus hyperodae N Z J Agric Res 43 227 233
17. NG Hairston FE Smith LB Slobodkin 1960 Community structure, population control, and competition Am Nat 94 421 425
18. Härri SA (2007) Fungal endosymbionts of grasses, and their effects on multitrophic interactions. PhD thesis, University of Zürich, Switzerland
19. Härri SA, Krauss J, Müller CB (2007) Can aphids learn to cope with the presence of endopyhtic fungi in their food plants? In: Popay AJ, Thom ER (eds) Proceedings of the 6th International Symposium on Fungal Endophytes of Grasses. New Zealand Grassland Association, Dunedin
20. HJ Henter S Via 1995 The potential for coevolution in a host-parasitoid system. 1. Genetic variation within an aphid population in susceptibility to a parasitic wasp Evolution 49 427 438
21. RD Holt JH Lawton 1993 Apparent competition and enemy-free space in insect host-parasitoid communities Am Nat 142 623 645
22. MG Hunt JA Newman 2005 Reduced herbivore resistance from a novel grass-endophyte association J Appl Ecol 42 762 769
23. MD Hunter 2003 Effects of plant quality on the population ecology of parasitoids Agric For Entomol 5 1 8
24. MD Hunter PW Price 1992 Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities Ecology 73 724 732
25. H Kagata T Ohgushi 2006 Bottom-up trophic cascades and material transfer in terrestrial food webs Ecol Res 21 26 34
26. Kazana E et al (2007) The cabbage aphid: a walking mustard oil bomb. Proc R Soc Lond B Biol Sci 274:2271-2277
27. AR Kraaijeveld HCJ Godfray 1997 Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster Nature 389 278 280
28. J Krauss 2007 Effects of fertilizer, fungal endophytes and plant cultivar on the performance of insect herbivores and their natural enemies Funct Ecol 21 107 116
29. K McCann 2007 Protecting biostructure Nature 446 29
30. B Meister J Krauss SA Härri MV Schneider CB Müller 2006 Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity Basic Appl Ecol 7 244 252
31. CB Müller HCJ Godfray 1999 Indirect interactions in aphid-parasitoid communities Res Popul Ecol 41 93 106
32. CB Müller J Krauss 2005 Symbiosis between grasses and asexual fungal endophytes Curr Opin Plant Biol 8 450 456
33. M Nakamura S Utsumi T Miki T Ohgushi 2005 Flood initiates bottom-up cascades in a tri-trophic system: host plant regrowth increases densities of a leaf beetle and its predators J Anim Ecol 74 683 691
34. PJ Ode 2006 Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions Annu Rev Entomol 51 163 185
35. M Omacini EJ Chaneton CM Ghersa CB Müller 2001 Symbiotic fungal endophytes control insect host-parasite interaction webs Nature 409 78 81
36. ML Pace JJ Cole SR Carpenter JF Kitchell 1999 Trophic cascades revealed in diverse ecosystems Trends Ecol Evol 14 483 488
37. ME Power WJ Matthews AJ Stewart 1985 Grazing minnows, piscivorous bass, and stream algae-dynamics of a strong interaction Ecology 66 1448 1456
38. C de Sassi CB Müller J Krauss 2006 Fungal plant endosymbionts alter life history and reproductive success of aphid predators Proc R Soc Lond B Biol Sci 273 1301 1306
39. CL Schardl A Leuchtmann MJ Spiering 2004 Symbioses of grasses with seedborne fungal endophytes Annu Rev Plant Biol 55 315 340
40. OJ Schmitz PA Hambäck AP Beckerman 2000 Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants Am Nat 155 141 153
41. R Soler TM Bezemer WH van der Putten LEM Vet JA Harvey 2005 Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality J Anim Ecol 74 1121 1130
42. SY Strauss 1991 Indirect effects in community ecology: their definition, study and importance Trends Ecol Evol 6 206 210
43. T Teder T Tammaru 2002 Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids Ecol Entomol 27 94 104
44. FJF van Veen RJ Morris HCJ Godfray 2006 Apparent competition, quantitative food webs, and the structure of phytophagous insect communities Annu Rev Entomol 51 187 208
45. Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
46. EE Werner SD Peacor 2003 A review of trait-mediated indirect interactions in ecological communities Ecology 84 1083 1100
47. JT Wootton 1993 Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications Am Nat 141 71 89