, Volume 108, Issue 4, pp 771–776 | Cite as

Aphid honeydew and its effect on the phyllosphere microflora of Picea abies (L.) Karst

  • Bernhard StadlerEmail author
  • Thomas Müller
Community Ecology


Aphids of the genus Cinara, feeding on Norway spruce, excrete copious amounts of honeydew, a carbon-rich waste product, which accumulates locally on needles and twigs. We investigated the role of honeydew as a potential source of energy which might promote the growth of micro-organisms in the phyllosphere of conifer trees. To approach this question, we followed the population dynamics of Cinara spp. in a natural forest stand over two seasons. We also studied the amounts of honeydew produced by individual aphids and identified potential parameters which might influence honeydew production. Finally, we determined the growth of micro-organisms on infested and uninfested needles of Norway spruce during the growing season. Confined to Picea abies, the investigated Cinara species only became abundant in midsummer, when needles and shoots were expanding. The populations showed only a single peak in abundance, the timing and magnitude of which may vary from year to year due to weather conditions, changes in plant quality in a yearly cycle or the impact of natural enemies. The amount of honeydew produced by individual aphids was dependent on the developmental stage of the aphid, the nutritional supply of its host plant and on the developmental state of the Norway spruce (e.g. bud burst, end of shoot extension). The presence of honeydew significantly increased the growth of bacteria, yeast and filamentous fungi on the surface of needles and there was a pronounced seasonal trend, with the highest abundance in midsummer correlating with the period of peak aphid abundance. Taken together, these findings indicate that aphids have an influence on microbial ecology in the phyllosphere of trees. The implication of our study, from interactions at the population level to effects and potential consequences for C and N fluxes at the level of forest ecosystems, is discussed.

Key words

Aphid honeydew Epiphytic micro-organisms Conifers Phyllosphere 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrews JH (1992) Biological control in the phyllosphere. Annu Rev Phytopathol 30: 603–635Google Scholar
  2. Bernstein ME, Carroll GC (1977) Microbial populations on Douglas fir needle surfaces. Microb Ecol 4: 41–52Google Scholar
  3. Brock TD, Madigan MT (1991) Biology of microorganisms, 6th edn. Prentice Hall, Englewood Cliffs, NJGoogle Scholar
  4. Blackman RL, Eastop VF (1994) Aphids on the world's trees. CAB International, WallingfordGoogle Scholar
  5. Bristow CM (1991) Why are so few aphids ant-tended? In: Huxley CR, Cutler DF (eds) Ant-plant-interactions. Oxford University Press, Oxford pp 104–119Google Scholar
  6. Campbell R (1977) Microbial ecology. (Basic microbiology, vol 5) Blackwell, OxfordGoogle Scholar
  7. Canny MJ (1990) Fine veins of dicotyledon leaves as sites for enrichment of solutes of the xylem sap. New Phytol 115: 511–516Google Scholar
  8. Carroll GC (1979) Needle microepiphytes in a Douglas fir canopy: biomass distribution patterns. Can J Bot 57: 1000–1007Google Scholar
  9. Choudhury D (1984) Aphids and plant fitness: a test of Owen and Wiegert's hypothesis. Oikos 43: 401–402Google Scholar
  10. Choudhury D (1985) Aphid honeydew: a re-appraisal of Owen and Wiegert's hypothesis. Oikos 45: 287–290Google Scholar
  11. Dighton J (1978) Effects of synthetic lime aphid honeydew on populations of soil organisms. Soil Biol Biochem 10: 369–376Google Scholar
  12. Dik AJ (1991) Interactions among fungicides, pathogens, yeast, and nutrients in the phyllosphere. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, Berlin Heidelberg New York, pp 412–429Google Scholar
  13. Dik AJ, Pelt JA van (1993) Interaction between phyllosphere yeasts, aphid honeydew and fungicide effectiveness in wheat under field conditions. Plant Pathol 41: 661–675Google Scholar
  14. Dik AJ, Fokkema NJ, Pelt JA van (1991) Consumption of aphid honeydew, a wheat yield reduction factor, by phyllosphere yeast under field conditions. Neth J Plant Pathol 97: 209–232Google Scholar
  15. Dixon AFG (1971a) The role of aphids in wood formation. I. The effect of the Sycamore aphid, Drepanosiphum plantanoides (Schr.) (Aphididae), on the growth of Sycamore, Acer pseudoplantanus (L.). J Appl Ecol 8: 165–179Google Scholar
  16. Dixon AFG (1971b) The role of aphids in wood formation. II. The effect of the Lime aphid, Eucallipterus tiliae L. (Aphididae), on the growth of Lime, Tilia vulgaris Hayne. J Appl Ecol 8: 393–399Google Scholar
  17. Drews G (1983) Mikrobiologisches Praktikum. Springer, Berlin Heidelberg, New YorkGoogle Scholar
  18. Eckloff W (1972) Beitrag zur Ökologie und forstlichen Bedeutung bienenwirtschaftlich wichtiger Rindenläuse. Z Angew Entomol 70:134–157Google Scholar
  19. Foster WA (1984) The distribution of the sea-lavender aphid Staticobium staticis on a marine saltmarsh and its effect on host plant fitness. Oikos 42: 97–104Google Scholar
  20. Heimbach U (1986) Freilanduntersuchungen zur Honigtauabgabe zweier Zierlausarten (Aphidina). J Appl Entomol 101: 396–413Google Scholar
  21. Grier CC, Vogt DJ (1990) Effects of aphid honeydew on soil nitrogen availability and net primary production in an Alnus rubra plantation in western Washington. Oikos 57: 114–118Google Scholar
  22. Johnson NE (1965) Reduced growth associated with infestations of Douglas-fir seedlings by Cinara species (Homoptera: Aphidae). Can Entomol 97: 113–119Google Scholar
  23. Kunkel H, Kloft WJ (1985) Die Honigtauerzeuger des Waldes. In: Kloft WJ, Kunkel H (eds) Waldtracht und Waldhonig in der Imkerei. Ehrenwirth, Munich, pp 48–264Google Scholar
  24. Llewellyn M (1975) The effect of the lime aphid (Eucallipterus tiliae L.) on the growth of the lime tree (Tilia x vulgaris Hayne). II. The primary production of saplings and mature trees, the energy drain imposed by the aphid populations and revised standard deviations of aphid population energy budgets. J Appl Ecol 12: 15–23Google Scholar
  25. Matzner E (1988) Der Stoffumsatz zweier Waldökosysteme im Solling. Ber Forschungszentrum Waldökosysteme Univ Göttingen, Reihe A, vol 40Google Scholar
  26. Maurizio A (1985) Honigtau-Honigtauhonig. In: Kloft WJ, Kunkel H (eds) Waldtracht und Waldhonig in der Imkerei. Ehrenwirth, Munich pp 268–295Google Scholar
  27. Müller H (1956) Können Honigtau liefernde Baumläuse (Lachnidae) ihre Wirtspflanzen schädigen? Z Angew Entomol 39: 168–177Google Scholar
  28. Müller H (1960) Der Honigtau als Nahrung der hügelbauenden Waldameisen. Entomophaga 5: 55–75Google Scholar
  29. Owen DF, Wiegert RG (1976) Do consumers maximize plant fitness? Oikos 27: 488–492Google Scholar
  30. Pearson J, Stewart GR (1993) The deposition of atmospheric ammonia and its effects on plants. New Phytol 125: 283–305Google Scholar
  31. Petelle M (1980) Aphids and melezitose: a test of Owen's 1978 hypothesis. Oikos 35: 127–128Google Scholar
  32. Pickett STA, Kolasa J, Jones CG (1994) Ecological understanding: the nature of theory and the theory of nature. Academic Press, OrlandoGoogle Scholar
  33. Qualls RG, Haines B, Swank W (1991) Fluxes of dissolved organic nutrients and humic substances in a deciduous forest. Ecology 72: 254–266Google Scholar
  34. Rodger G, Blakeman JP (1984) Microbial colonization and uptake of 14C label on leaves of Sycamore. Trans B Mycol Soc 82: 45–51Google Scholar
  35. Scheuer S (1964) Zur Biologie einiger Fichten bewohnender Lachnidenarten (Homoptera, Aphidina) Z Angew Entomol 53: 153–178Google Scholar
  36. Schlegel HG (1992) Allgemeine Mikrobiologie. 7th edn. Thieme, StuttgartGoogle Scholar
  37. Schulze E-D, Vries W de, Hauhs M, Rosen K, Rasmussen L, Tamm CO, Nilsson J (1989) Critical loads for nitrogen deposition on forest ecosystems. Water Air Soil Pollut 48: 451–456Google Scholar
  38. Schulze E-D, Zwölfer H (1994) Fluxes in ecosystems. In: Schulze E-D (ed) Flux control in biological systems. Academic Press, New York, pp 421–445Google Scholar
  39. Stadler B (1996) The relative importance of host plants, natural enemies and ants in the evolution of life-history characters in aphids. Ecol Stud (in press)Google Scholar
  40. Tukey HB, Tukey HB Jr (1969) The leaching of materials from leaves. In: Linser H (ed) Handbuch der Pflanzenernährung und Düngung, vol 1. Springer, Vienna New York, pp 585–594Google Scholar
  41. Zoebelein G (1954) Versuche zur Feststellung des Honigtauertrages von Fichtenbeständen mit Hilfe von Waldameisen. Z Angew Enomol 36: 358–362Google Scholar
  42. Zoebelein G (1956) Der Honigtau als Nahrung der Insekten. Z Angew Entomol 38: 369–416Google Scholar
  43. Zwölfer W (1952) Die Waldbienenweide und ihre Nutzung als forstentomologisches Problem. Verhandl Dtsch Ges Angew Entomol auf d 12. Mitglv Frankfurt 1952: 164–168Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  1. 1.Bayreuth Institute for Terrestrial Ecosystem ResearchUniversity of BayreuthBayreuthGermany
  2. 2.Centre for Agricultural Landscape and Land Use Research, MünchebergInstitute of Microbial Ecology and Soil BiologyPaulinenaueGermany

Personalised recommendations