Skip to main content
Log in

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

  • Community Ecology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Andrews JH (1992) Biological control in the phyllosphere. Annu Rev Phytopathol 30: 603–635

    Google Scholar 

  • Bernstein ME, Carroll GC (1977) Microbial populations on Douglas fir needle surfaces. Microb Ecol 4: 41–52

    Google Scholar 

  • Brock TD, Madigan MT (1991) Biology of microorganisms, 6th edn. Prentice Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Blackman RL, Eastop VF (1994) Aphids on the world's trees. CAB International, Wallingford

    Google Scholar 

  • Bristow CM (1991) Why are so few aphids ant-tended? In: Huxley CR, Cutler DF (eds) Ant-plant-interactions. Oxford University Press, Oxford pp 104–119

    Google Scholar 

  • Campbell R (1977) Microbial ecology. (Basic microbiology, vol 5) Blackwell, Oxford

    Google Scholar 

  • Canny MJ (1990) Fine veins of dicotyledon leaves as sites for enrichment of solutes of the xylem sap. New Phytol 115: 511–516

    Google Scholar 

  • Carroll GC (1979) Needle microepiphytes in a Douglas fir canopy: biomass distribution patterns. Can J Bot 57: 1000–1007

    Google Scholar 

  • Choudhury D (1984) Aphids and plant fitness: a test of Owen and Wiegert's hypothesis. Oikos 43: 401–402

    Google Scholar 

  • Choudhury D (1985) Aphid honeydew: a re-appraisal of Owen and Wiegert's hypothesis. Oikos 45: 287–290

    Google Scholar 

  • Dighton J (1978) Effects of synthetic lime aphid honeydew on populations of soil organisms. Soil Biol Biochem 10: 369–376

    Google Scholar 

  • 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 412–429

    Google Scholar 

  • Dik AJ, Pelt JA van (1993) Interaction between phyllosphere yeasts, aphid honeydew and fungicide effectiveness in wheat under field conditions. Plant Pathol 41: 661–675

    Google Scholar 

  • 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: 209–232

    Google Scholar 

  • 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: 165–179

    Google Scholar 

  • 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: 393–399

    Google Scholar 

  • Drews G (1983) Mikrobiologisches Praktikum. Springer, Berlin Heidelberg, New York

    Google Scholar 

  • Eckloff W (1972) Beitrag zur Ökologie und forstlichen Bedeutung bienenwirtschaftlich wichtiger Rindenläuse. Z Angew Entomol 70:134–157

    Google Scholar 

  • 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: 97–104

    Google Scholar 

  • Heimbach U (1986) Freilanduntersuchungen zur Honigtauabgabe zweier Zierlausarten (Aphidina). J Appl Entomol 101: 396–413

    Google Scholar 

  • 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: 114–118

    Google Scholar 

  • Johnson NE (1965) Reduced growth associated with infestations of Douglas-fir seedlings by Cinara species (Homoptera: Aphidae). Can Entomol 97: 113–119

    Google Scholar 

  • Kunkel H, Kloft WJ (1985) Die Honigtauerzeuger des Waldes. In: Kloft WJ, Kunkel H (eds) Waldtracht und Waldhonig in der Imkerei. Ehrenwirth, Munich, pp 48–264

    Google Scholar 

  • 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: 15–23

    Google Scholar 

  • Matzner E (1988) Der Stoffumsatz zweier Waldökosysteme im Solling. Ber Forschungszentrum Waldökosysteme Univ Göttingen, Reihe A, vol 40

  • Maurizio A (1985) Honigtau-Honigtauhonig. In: Kloft WJ, Kunkel H (eds) Waldtracht und Waldhonig in der Imkerei. Ehrenwirth, Munich pp 268–295

    Google Scholar 

  • Müller H (1956) Können Honigtau liefernde Baumläuse (Lachnidae) ihre Wirtspflanzen schädigen? Z Angew Entomol 39: 168–177

    Google Scholar 

  • Müller H (1960) Der Honigtau als Nahrung der hügelbauenden Waldameisen. Entomophaga 5: 55–75

    Google Scholar 

  • Owen DF, Wiegert RG (1976) Do consumers maximize plant fitness? Oikos 27: 488–492

    Google Scholar 

  • Pearson J, Stewart GR (1993) The deposition of atmospheric ammonia and its effects on plants. New Phytol 125: 283–305

    Google Scholar 

  • Petelle M (1980) Aphids and melezitose: a test of Owen's 1978 hypothesis. Oikos 35: 127–128

    Google Scholar 

  • Pickett STA, Kolasa J, Jones CG (1994) Ecological understanding: the nature of theory and the theory of nature. Academic Press, Orlando

    Google Scholar 

  • Qualls RG, Haines B, Swank W (1991) Fluxes of dissolved organic nutrients and humic substances in a deciduous forest. Ecology 72: 254–266

    Google Scholar 

  • Rodger G, Blakeman JP (1984) Microbial colonization and uptake of 14C label on leaves of Sycamore. Trans B Mycol Soc 82: 45–51

    Google Scholar 

  • Scheuer S (1964) Zur Biologie einiger Fichten bewohnender Lachnidenarten (Homoptera, Aphidina) Z Angew Entomol 53: 153–178

    Google Scholar 

  • Schlegel HG (1992) Allgemeine Mikrobiologie. 7th edn. Thieme, Stuttgart

    Google Scholar 

  • 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: 451–456

    Google Scholar 

  • Schulze E-D, Zwölfer H (1994) Fluxes in ecosystems. In: Schulze E-D (ed) Flux control in biological systems. Academic Press, New York, pp 421–445

    Google Scholar 

  • 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)

  • 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 585–594

    Google Scholar 

  • Zoebelein G (1954) Versuche zur Feststellung des Honigtauertrages von Fichtenbeständen mit Hilfe von Waldameisen. Z Angew Enomol 36: 358–362

    Google Scholar 

  • Zoebelein G (1956) Der Honigtau als Nahrung der Insekten. Z Angew Entomol 38: 369–416

    Google Scholar 

  • Zwölfer W (1952) Die Waldbienenweide und ihre Nutzung als forstentomologisches Problem. Verhandl Dtsch Ges Angew Entomol auf d 12. Mitglv Frankfurt 1952: 164–168

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bernhard Stadler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stadler, B., Müller, T. Aphid honeydew and its effect on the phyllosphere microflora of Picea abies (L.) Karst. Oecologia 108, 771–776 (1996). https://doi.org/10.1007/BF00329054

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00329054

Key words

Navigation