Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid

Abstract

The role of indirect interactions in structuring communities is becoming increasingly recognised. Plant fungi can bring about changes in plant chemistry which may affect insect herbivores that share the same plant, and hence the two may interact indirectly. This study investigated the indirect effects of a fungal pathogen (Marssonina betulae) of silver birch (Betula pendula) on an aphid (Euceraphis betulae), and the processes underpinning the interaction. There was a strong positive association between natural populations of the aphid and leaves bearing high fungal infection. In choice tests, significantly more aphids settled on leaves inoculated with the fungus than on asymptomatic leaves. Individual aphids reared on inoculated leaves were heavier, possessed longer hind tibiae and displayed enhanced embryo development compared with aphids reared on asymptomatic leaves; population growth rate was also positively correlated with fungal infection when groups of aphids were reared on inoculated branches. Changes in leaf chemistry were associated with fungal infection with inoculated leaves containing higher concentrations of free-amino acids. This may reflect a plant-initiated response to fungal attack in which free amino acids from the degradation of mesophyll cells are translocated out of infected leaves via the phloem. These changes in plant chemistry are similar to those occurring during leaf senescence, and are proposed as the mechanistic basis for the positive interaction between the fungus and aphid.

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References

  1. Adams D, Douglas AE (1997) How symbiotic bacteria influence plant utilisation by the polyphagous aphid, Aphis fabae. Oecologia 110:528–532

    Article  Google Scholar 

  2. Bailey JP, Mansfield JA (1982) Phytoalexins. Blackie, London

  3. Barbosa P (1991) Plant pathogens and nonvector herbivores. In: Barbosa P, Krischik VA, Jones CJ (eds) Microbial mediation of plant-herbivore interactions. Wiley, New York, pp 341–382

  4. Bennell AP, Millar CS (1984) Fungal pathogens of birch in Britain. Proc R Soc Edinburgh Ser B Biol Sci 85:153–167

    Google Scholar 

  5. Bergelson J, Fowler SV, Hartley SE (1986) The effects of foliage damage on case bearing moth larvae, Coleophora serratella , feeding on birch. Ecol Entomol 11:241–250

    Google Scholar 

  6. Blackman RL (1977) The existence of two species of Euceraphis (Homoptera: Aphididae) on birch in Western Europe, and a key to European and North American species of the genus. Syst Entomol 2:1–8

    Google Scholar 

  7. Blackman RL, Eastop VE (1994) Aphids on the world's trees. CAB International, Oxford

  8. Breen JP (1994) Acremonium endophyte interactions with enhanced plant-resistance to insects. Annu Rev Entomol 39:401–423

    Article  Google Scholar 

  9. Chapin FS, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64:376–391

    CAS  Google Scholar 

  10. Cronin JT, Abrahamson WG (2001) Goldenrod stem galler preference and performance: effects of multiple herbivores and plant genotypes. Oecologia 127:87–96

    Google Scholar 

  11. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects - competition reexamined and resurrected. Annu Rev Entomol 40:297–331

    Article  CAS  Google Scholar 

  12. Denno RF et al. (2000) Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores. Ecology 81:1814–1827

    Google Scholar 

  13. Dicke M (1994) Local and systemic production of volatile herbivore-induced terpenoids—their role in plant-carnivore mutualism. J Plant Physiol 143:465–472

    CAS  Google Scholar 

  14. Dixon AFG (1998) Aphid ecology. An optimization approach. Chapman and Hall, London

  15. Dixon AFG, Wellings PW, Carter C, Nichols JFA (1993) The role of food quality and competition in shaping the seasonal cycle in the reproductive activity of the sycamore aphid. Oecologia 95:89–92

    Google Scholar 

  16. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847

    Google Scholar 

  17. Fisher AEI, Hartley SE, Young M (2000) Direct and indirect competitive effects of foliage feeding guilds on the performance of the birch leaf-miner Eriocrania. J Anim Ecol 69:165–176

    Article  Google Scholar 

  18. Fowler SV, Lawton JH (1984) Foliage preferences of birch herbivores: a field manipulation experiment. Oikos 42:239–248

    Google Scholar 

  19. Fowler SV, Macgarvin M (1986) The effects of leaf damage on the performance of insect herbivores on Birch, Betula pubescens. J Anim Ecol 55:565–573

    Google Scholar 

  20. Fox JW, Olsen E (2000) Food web structure and the strength of transient indirect effects. Oikos 90:219–226

    Google Scholar 

  21. Gange AC (1996) Positive effects of endophyte infection on sycamore aphids. Oikos 75:500–510

    Google Scholar 

  22. Hajek AE, Dahlsten DL (1986) Coexistence of 3 species of leaf-feeding aphids (Homoptera) on Betula pendula. Oecologia 68:380–386

    Google Scholar 

  23. Hajek AE, Dahlsten DL (1988) Distribution and dynamics of aphid (Homoptera, Drepanosiphidae) populations on Betula pendula in northern California. Hilgardia 56:1–33

    Google Scholar 

  24. Hammon KE, Faeth SH (1992) Ecology of plant-herbivore communities: a fungal component? Nat Toxins 1:197–208

    CAS  PubMed  Google Scholar 

  25. Hartley SE, Firn RD (1989) Phenolic biosynthesis, leaf damage, and insect herbivory in Birch ( Betula pendula). J Chem Ecol 15:275–283

    CAS  Google Scholar 

  26. Hartley SE, Jones CG (1997) Plant chemistry and herbivory, or Why the world is green. In: Crawley MJ (ed) Plant ecology. Blackwell Science, Oxford, pp 284–324

  27. Hartley SE, Lawton JH (1987) Effects of different types of damage on the chemistry of birch foliage, and the responses of birch feeding insects. Oecologia 74:432–437

    Google Scholar 

  28. Hatcher PE (1995) 3-Way Interactions between plant-pathogenic fungi, herbivorous insects and their host plants. Biol Rev Cambridge Phil Soc 70:639–694

    Google Scholar 

  29. Haukioja E, Niemela P (1979) Birch leaves as a resource for herbivores: seasonal occurrence of increased resistance in foliage after mechanical damage of adjacent leaves. Oecologia 39:151–159

    Google Scholar 

  30. Haukioja E, Niemela P, Siren S (1985) Foliage phenols and nitrogen in relation to growth, insect damage, and ability to recover after defoliation, in the mountain birch Betula pubsecens ssp. tortuosa. Oecologia 65:214–222

    Google Scholar 

  31. Haukioja E, Ruohomaki K, Senn J, Suomela J, Walls M (1990) Consequences of herbivory in the mountain Birch ( Betula pubescens ssp tortuosa) - importance of the functional organization of the tree. Oecologia 82:238–247

    Google Scholar 

  32. Johnson SN, Mayhew PJ, Douglas AE, Hartley SE (2002) Insects as leaf engineers—can leaf-miners alter leaf structure for birch aphids? Funct Ecol 16:575–584

    Article  Google Scholar 

  33. Jones BN, Paabo S, Stein S (1981) Amino-acid-analysis and enzymatic sequence determination of peptides by an improved ortho-phthaldialdehyde pre-column labeling procedure. J Liquid Chromatogr 4:565–586

    CAS  Google Scholar 

  34. Karban R, Myers JH (1989) Induced plant responses to herbivory. Annu Rev Ecol Syst 20:331–348

    Article  Google Scholar 

  35. Kerslake JE, Woodin SJ, Hartley SE (1998) Effects of carbon dioxide and nitrogen enrichment on a plant- insect interaction: the quality of Calluna vulgaris as a host for Operophtera brumata. New Phytol 140:43–53

    Article  Google Scholar 

  36. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    CAS  PubMed  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Kruess A (2002) Indirect interaction between a fungal plant pathogen and a herbivorous beetle of the weed Cirsium arvense. Oecologia 130:563–569

    Google Scholar 

  39. Kurkela T (1995) Fungi associated with leaf anthracnoses of birch. In: Capretti P, Heiniger U, Stephan R (eds) Shoot and foliage diseases in forest trees. Universita degli Studi di Firenze, Vallombrosa, Florence, Italy, pp 91–95

  40. Leather SR, Wellings PW (1981) Ovariole number and fecundity in aphids. Entomol Exp Appl 30:128–133

    Google Scholar 

  41. Leather SR, Watt AD, Forrest GI (1987) Insect induced chemical changes in young lodgepole pine ( Pinus contorta)—the effect of previous defoliation on oviposition, growth and survival of the pine beauty moth, Panolis flammea. Ecol Entomol 12:275–281

    Google Scholar 

  42. Lehtilä K, Haukioja E, Kaitaniemi P, Laine KA (2000) Allocation of resources within mountain birch canopy after simulated winter browsing. Oikos 90:160–170

    Google Scholar 

  43. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C.

  44. Martin MA, Cappuccino N, Ducharme D (1994) Performance of Symydobius americanus (Homoptera, Aphididae) on paper birch grazed by caterpillars. Ecol Entomol 19:6–10

    CAS  Google Scholar 

  45. Martin MM (1979) Biochemical implications of insect mycophagy. Biol Rev 54:1–21

    CAS  Google Scholar 

  46. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

    Google Scholar 

  47. Moran PJ (1998) Plant-mediated interactions between insects and a fungal plant pathogen and the role of plant chemical responses to infection. Oecologia 115:523–530

    Article  Google Scholar 

  48. Neuvonen S, Lindgren M (1987) The effect of simulated acid-rain on performance of the aphid Euceraphis betulae (Koch) on silver birch. Oecologia 74:77–80

    Google Scholar 

  49. Omacini M, Chaneton EJ, Ghersa CM, Muller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81

    Article  CAS  PubMed  Google Scholar 

  50. Ossipov V, Haukioja E, Ossipova S, Hanhimaki S, Pihlaja K (2001) Phenolic and phenolic-related factors as determinants of suitability of mountain birch leaves to an herbivorous insect. Biochem Syst Ecol 29:223–240

    CAS  PubMed  Google Scholar 

  51. Paavolainen L, Hantula J, Kurkela T (2000) Pyrenopeziza betulicola and an anamorphic fungus occurring in leaf spots of birch. Mycol Res 104:611–617

    Article  Google Scholar 

  52. Pare PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95:13971–13975

    Google Scholar 

  53. Peace TR (1962) Pathology of trees and shrubs. Oxford University Press, Oxford

  54. Pesel E, Poehling H-M (1988) Influence of abiotic (water deficient) and biotic (powdery mildew, Erysiphe graminis f. sp. tritici) stresses on the population dynamics of the cereal aphids Metopolophium dirhodum Walk. and Sitobion avenae F. (Homoptera: Aphididae). Mitt Dtsch Ges Allg Angew Entomol 6:531–536

    Google Scholar 

  55. Petersen MK, Sandstrom JP (2001) Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Funct Ecol 15:525–534

    Article  Google Scholar 

  56. Phillips DH, Burdekin DA (1992) Diseases of forest and ornamental trees. Macmillan, London

  57. Polis GA (1998) Ecology—stability is woven by complex webs. Nature 395:744–745

    Article  Google Scholar 

  58. Raffa KF, Smalley EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle fungal complexes. Oecologia 102:285–295

    Google Scholar 

  59. Raven JA (1983) Phytophages of xylem and phloem—a comparison of animal and plant sap-feeders. Adv Ecol Res 13:135–234

    Google Scholar 

  60. Redlin SC (1995) Classification and pathogenicity of the birch anthracnose fungus. In: Capretti P, Heiniger U, Stephan R (eds) Shoot and foliage diseases in forest trees. Universita degli Studi di Firenze, Vallombrosa, Florence, Italy, pp 86–90

  61. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  62. SAS Institute (1999) SAS/STAT User's Guide, Version 8. SAS Institute, Cary, N.C.

  63. Schall R (1991) Estimation in generalized linear-models with random effects. Biometrika 78:719–727

    Google Scholar 

  64. Sequeira R, Dixon AFG (1997) Population dynamics of tree-dwelling aphids: the importance of seasonality and time scale. Ecology 78:2603–2610

    Google Scholar 

  65. Sinclair WA, Lyon HH, Johnson WT (1987) Diseases of trees and shrubs. Cornell University Press, London

  66. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York

  67. Southwood TRE, Moran VC, Kennedy CEJ (1982) The richness, abundance and biomass of the arthropod communities on trees. J Anim Ecol 51:635–649

    Google Scholar 

  68. Stadler B (1995) Adaptive allocation of resources and life-history trade-offs in aphids relative to plant-quality. Oecologia 102:246–254

    Google Scholar 

  69. Staley JT (1999) Insect herbivores on birch: interactions between the phloem-feeding and leaf-chewing guilds, mediated by the host plant. MSc Thesis, University of Aberdeen, Aberdeen

    Google Scholar 

  70. Thomas H, Stoddart JL (1980) Leaf senescence. Annu Rev Plant Physiol 31:83–111

    CAS  Google Scholar 

  71. Todd GW, Getahun A, Cress DC (1971) Resistance in barley to greenbug, Schizaphis graminum. 1. Toxicity of phenolic and flavonoid compounds and related substances. Ann Entomol Soc Am 64:718–722

    CAS  Google Scholar 

  72. Valladares GR, Hartley SE (1994) Effects of scale on detecting interactions between Coleophora and Eriocrania leaf-miners. Ecol Entomol 19:257–262

    Google Scholar 

  73. Vanderplank JE (1982) Host-pathogen interactions in plant disease. Academic Press, New York

  74. Waring CL, Cobb NS (1992) The impact of plant stress on herbivore population dynamics. In: Bernays EA (ed) Insect-plant interactions. CRC, Boca Raton

  75. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, Oxford

  76. Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL (2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol Plant-Microbe Interact 13:1027–1033

    CAS  Google Scholar 

  77. Wilson D, Faeth SH (2001) Do fungal endophytes result in selection for leafminer ovipositional preference? Ecology 82:1097–1111

    Google Scholar 

  78. Zebitz CPW (1988) Effects of broad bean rust on host plant quality of Vicia faba to Aphis fabae. Med Fac Landbouw 53:1203–1211

    Google Scholar 

  79. Zebitz CPW, Kehlenbeck H (1991) Performance of Aphis fabae on chocolate spot disease-infected Faba bean plants. Phytoparasitica 19:113–119

    Google Scholar 

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Acknowledgements

We are grateful to Dr. Peter Mayhew and Dr. Allan Watt for their invaluable critical comments on this manuscript and to Dr. David Elston of Biomathematics and Statistics (Scotland) for statistical guidance. Dr. Alison Karley, Lyn Minto and Kim Simpson are thanked for their assistance with HPLC analysis, as is Robert Strang-Steele for permission to use Dalhaikie Flat for field trials. This research was funded by a NERC PhD Studentship (GT04/98/302/TS).

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Correspondence to Scott N. Johnson.

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Johnson, S.N., Douglas, A.E., Woodward, S. et al. Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid. Oecologia 134, 388–396 (2003). https://doi.org/10.1007/s00442-002-1139-6

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Keywords

  • Amino acids
  • Indirect interactions
  • Leaf spot disease
  • Phenolics