Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1651, 2008, Pages 2627-2632

  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

Asaphes vulgaris; Bottom up cascade; Endophytic fungi; Mummy parasitoids; Neotyphodium lolii; Oviposition strategy

Indexed keywords

TOXIN;

APHID; BOTTOM-UP CONTROL; ENDOPHYTE; ENDOSYMBIONT; FOOD CHAIN; FUNGUS; HERBIVORE; HOST QUALITY; HOST SELECTION; HOST-PARASITOID INTERACTION; OVIPOSITION; REPRODUCTIVE STRATEGY; SENSITIVITY ANALYSIS;

ANIMAL BEHAVIOR; APHID; ARTICLE; CONTROLLED STUDY; EGG LAYING; ENDOPHYTE; ENDOSYMBIONT; ENDOSYMBIOSIS; FEMALE; FOOD CHAIN; HERBIVORE; HOST SELECTION; LIFESPAN; MALE; NONHUMAN; PARASITOID; PLANT FUNGUS INTERACTION; PRIORITY JOURNAL;

APHIDIDAE; ASAPHES VULGARIS; FUNGI; NEOTYPHODIUM LOLII;

EID: 54249135327     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0594     Document Type: Article

References (39)

1. Arnold, A. E. & Lutzoni, F. 2007 Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88, 541-549. (doi:10.1890/05-1459)
2. Brodeur, J. 2000 Host specificity and trophic relationships of hyperparasitoids. In Parasitoid population biology (eds M. E. Hochberg & A. R. Ives), pp. 163-183. Princeton, NJ: Princeton University Press.
3. Buitenhuis, R., McNeil, J. N., Boivin, G. & Brodeur, J. 2004 The role of honeydew in host searching of aphid hyperparasitoids. J. Chem. Ecol. 30, 273-285. (doi:10.1023/b:joec.0000017977.39957.97)
4. Bultman, T. L., Borowicz, K. L., Schneble, R. M., Coudron, T. A. & Bush, L. P. 1997 Effect of a fungal endophyte on the growth and survival of two Euplectrus parasitoids. Oikos 78, 170-176. (doi:10.2307/3545812)
5. Charnov, E. L., Los- den Hartogh, R. L., Jones, W. T. & van den Assem, J. 1981 Sex ratio evolution in a variable environment. Nature 289, 27-33. (doi:10.1038/289027a0)
6. Chow, A. & Mackauer, M. 1999 Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species. J. Appl. Entomol. 123, 83-91. (doi:10.1046/j.1439-0418.1999.00322.x)
7. Christiansen-Weniger, P. 1992 Wirt-Parasitoid-Beziehung zwischen Blattlausprimärparasitoiden und den Blattlaushyperparasitoiden Asaphes vulgaris Wlk. und Asaphes suspensus (Nees)(Hymenoptera: Pteromalidae). PhD thesis Christian-Albrechts-Universität zu Kiel, Kiel, Germany.
8. Clay, K. 1990 Fungal endophytes of grasses. Annu. Rev. Ecol. Syst. 21, 275-297. (doi:10.1146/annurev.es.21.110190.001423)
9. de Sassi, C., Müller, C. B. & Krauss, J. 2006 Fungal plant endosymbionts alter life history and reproductive success of aphid predators. Proc. R. Soc. B 273, 1301-1306. (doi:10.1098/rspb.2005.3442)
10. Douloumpaka, S. & van Emden, H. F. 2003 A maternal influence on the conditioning to plant cues of Aphidius colemani Viereck, parasitizing the aphid Myzus persicae Sulzer. Physiol. Entomol. 28, 108-113. (doi:10.1046/j.1365-3032.2003.00323.x)
11. Godfray, H. C. J. 1994 Parasitoids. Behavioral and evolutionary ecology. Monographs in Behavior and Ecology. Princeton, NJ: Princeton University Press.
12. Härri, S. A. 2007 Fungal endosymbionts of grasses, and their effects on multitrophic interactions. PhD thesis, University of Zürich, Zürich, Switzerland.
13. Harvey, J. A. 2008 Comparing and contrasting development and reproductive strategies in the pupal hyperparasitoids Lysibia nana and Gelis agilis (Hymenoptera: Ichneumonidae). Evol. Ecol. 22, 153-166. (doi:10.1007/s10682-007-9164-x)
14. Harvey, J. A., van Dam, N. M. & Gols, R. 2003 Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J. Anim. Ecol. 72, 520-531. (doi:10.1046/j.1365-2656.2003.00722.x)
15. Heimpel, G. E., Rosenheim, J. A. & Mangel, M. 1996 Egg limitation, host quality, and dynamic behavior by a parasitoid in the field. Ecology 77, 2410-2420. (doi:10.2307/2265742)
16. Iwasa, Y., Suzuki, Y. & Matsuda, H. 1984 Theory of oviposition strategy of parasitoids - 1. Effect of mortality and limited egg number. Theor. Popul. Biol. 26, 205-227. (doi:10.1016/0040-5809(84)90030- 3)
17. Jervis, M. A. & Kidd, N. A. C. 1986 Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. Camb. Phil. Soc. 61, 395-434. (doi:10.1111/j.1469-185X.1986.tb00660.x)
18. Jervis, M. A., Ellers, J. & Harvey, J. A. 2008 Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53, 361-385. (doi:10.1146/annurev.ento.53.103106.093433)
19. Kidd, N. A. C. & Jervis, M. A. 1991 Host-feeding and oviposition strategies of parasitoids in relation to host stage. Res. Popul. Ecol. 33, 13-28. (doi:10.1007/bf02514570)
20. Müller, C. B. & Krauss, J. 2005 Symbiosis between grasses and asexual fungal endophytes. Curr. Opin. Plant Biol. 8, 450-456. (doi:10.1016/j.pbi.2005.05.007)
21. Müller, C. B., Adriaanse, I. C. T., Belshaw, R. & Godfray, H. C. J. 1999 The structure of an aphid-parasitoid community. J. Anim. Ecol. 68, 346-370. (doi:10.1046/j.1365-2656.1999.00288.x)
22. Ohgushi, T., Craig, T. P. & Price, P. W. 2007 Indirect interaction webs: an introduction. In Ecological communities: plant mediation in indirect interaction webs (eds T. Ohgushi, T. P. Craig & P. W. Price), pp. 3-15. Cambridge, UK: Cambridge University Press.
23. 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. (doi:10.1038/35051070)
24. Pimm, S. L. & Lawton, J. H. 1977 Number of trophic levels in ecological communities. Nature 268, 329-331. (doi:10.1038/ 268329a0)
25. Pinheiro, J. C. & Bates, D. M. 2000 Mixed-effects models in S and S-PLUS. Statistics and computing. New York, NY: Springer.
26. Polis, G. A. & Strong, D. R. 1996 Food web complexity and community dynamics. Am. Nat. 147, 813-846. (doi:10.1086/285880)
27. Quicke, D. L. J. 1997 Parasitic wasps. London, UK: Chapman & Hall.
28. Rosenheim, J. A. 1998 Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43, 421-447. (doi:10.1146/annurev.ento.43.1.421)
29. Rosenheim, J. A., Heimpel, G. E. & Mangel, M. 2000 Egg maturation, egg resorption and the costliness of transient egg limitation in insects. Proc. R. Soc. B 267, 1565-1573. (doi:10.1098/rspb.2000.1179)
30. Saikkonen, K., Ahlholm, J., Helander, M., Lehtimäki, S. & Niemeläinen, O. 2000 Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23, 360-366. (doi:10.1034/j.1600-0587.2000.d01- 1645.x)
31. Soler, R., Bezemer, T. M., van der Putten, W. H., Vet, L. E. M. & Harvey, J. A. 2005 Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol. 74, 1121-1130. (doi:10.1111/j.1365-2656.2005.01006.x)
32. Sullivan, D. J. 1987 Insect hyperparasitism. Annu. Rev. Entomol. 32, 49-70. (doi:10.1146/annurev.en.32.010187.000405)
33. Sullivan, D. J. & Völkl, W. 1999 Hyperparasitism: multitrophic ecology and behavior. Annu. Rev. Entomol. 44, 291-315. (doi:10.1146/annurev.ento.44.1.291)
34. van Emden, H. F., Sponagl, B., Wagner, E., Baker, T., Ganguly, S. & Douloumpaka, S. 1996 Hopkins 'host selection principle', another nail in its coffin. Physiol. Entomol. 21, 325-328. (doi:10.1111/j.1365-3032. 1996.tb00873.x)
35. van Nouhuys, S. & Hanski, I. 2002 Multitrophic interactions in space: metacommunity dynamics in fragmented landscapes. In Multitrophic level interactions (eds T. Tscharntke & B. A. Hawkins), pp. 124-147. Cambridge, UK: Cambridge University Press.
36. Venables, W. N. & Ripley, B. D. 2002 Modern applied statistics with S. New York, NY: Springer.
37. Vet, L. E. M., Lewis, W. J., Papaj, D. R. & van Lenteren, J. C. 1990 A variable-response model for parasitoid foraging behavior. J. Insect Behav. 3, 471-490. (doi:10.1007/BF01052012)
38. Vinson, S. B. 1976 Host selection by insect parasitoids. Annu. Rev. Entomol. 21, 109-133. (doi:10.1146/annurev.en.21.010176.000545)
39. Zabalgogeazcoa, I., Vázquez de Aldana, B. R., García Ciudad, A. & García Criado, B. 2003 Fungal endophytes in grasses from semi-arid permanent grasslands of western Spain. Grass Forage Sci. 58, 94-97. (doi:10.1046/j.1365-2494.2003.00352.x)