Skip to main content

Advertisement

SpringerLink
Log in

Long-term experimental warming, shading and nutrient addition affect the concentration of phenolic compounds in arctic-alpine deciduous and evergreen dwarf shrubs

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Environmental changes are likely to alter the chemical composition of plant tissues, including content and concentrations of secondary compounds, and thereby affect the food sources of herbivores. After 10 years of experimental increase of temperature, nutrient levels and light attenuation in a sub-arctic, alpine ecosystem, we investigated the effects on carbon based secondary compounds (CBSC) and nitrogen in one dominant deciduous dwarf shrub, Salix herbacea × polaris and two dominant evergreen dwarf shrubs, Cassiope tetragona and Vaccinium vitis-idaea throughout one growing season. The main aims were to compare the seasonal course and treatment effects on CBSC among the species, life forms and leaf cohorts and to examine whether the responses in different CBSC were consistent across compounds. The changes in leaf chemistry both during the season and in response to the treatments were higher in S. herbacea × polaris than in the corresponding current year’s leaf cohort of the evergreen C. tetragona. The changes were also much higher than in the 1-year-old leaves of the two evergreens probably due to differences in dilution and turnover of CBSC in growing and mature leaves paired with different rates of allocation. Most low molecular weight phenolics in the current year’s leaves decreased in all treatments. Condensed tannins and the tannin-to-N ratio, however, either increased or decreased, and the strength and even direction of the responses varied among the species and leaf cohorts, supporting views of influential factors additional to resource-based or developmental controls, as e.g. species specific or genetic controls of CBSC. The results indicate that there is no common response to environmental changes across species and substances. However, the pronounced treatment responses imply that the quality of the herbivore forage is likely to be strongly affected in a changing arctic environment, although both the direction and strength of the responses will be different among plant species, tissue types and substances.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • ACIA (2004) Impacts of a warming Arctic. Arctic Climate Impact Assessment. Cambridge Univ Press, Cambridge, pp 138

  • AMAP (1998) AMAP Assessment Report: Arctic Pollution Issues. Arctic Monitoring and Assessment Programme (AMAP), Oslo, pp 859

  • Anisimov O, Fitzharris B, Hagen JO, Jefferies R, Marchant H, Nelson F, Prowse T, Vaughan DG (2001) Polar Regions (Arctic and Antarctic). In: McCarthy JJ, Canziani OF, Leary NA, Dokken DJ, White KS (eds) Impact, Adaptations, and Vulnerability, Contribution of Working Group II to the third assessment report of the Intergovernmental Panel on Climate Change. Cambridge Univ Press, Cambridge, pp 801–841

    Google Scholar 

  • Berenbaum MR, Zangerl AR (1992) Genetics of secondary metabolism and herbivore resistance in plants. In: Rosenthal GA (ed) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 415–438

    Google Scholar 

  • Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368

    Article  CAS  Google Scholar 

  • Burns RE (1971) Method for estimation of tannin in grain Sorghum. Agron J 63:511–512

    Article  CAS  Google Scholar 

  • Chapin FS III, Bret-Harte MS, Hobbie SE, Zong H (1996) Plant functional types as predictors of transient responses of arctic vegetation to global change. J Veg Sci 7:347–358

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Fraenkel GS (1959) The raison d’être of secondary plant substances. Science 129:1466–1470

    Article  PubMed  CAS  Google Scholar 

  • Gershenzon J (1994) The cost of plant chemical defense against herbivory: a biochemical perspective. In: Bernays EA (ed) Insect-plant interaction. CRC Press, Boca Raton, pp 105–173

    Google Scholar 

  • Graglia E, Jonasson S, Michelsen A, Schmidt IK (1997) Effects of shading, nutrient application and warming on leaf growth and shoot densities of dwarf shrubs in two arctic-alpine plant communities. Ecoscience 4:191–198

    Google Scholar 

  • Graglia E, Jonasson S, Michelsen A, Schmidt IK, Havström M, Gustavsson L (2001) Effects of environmental perturbations on abundance of subarctic plants after three, seven, and ten years of treatments. Ecography 24:5–12

    Article  Google Scholar 

  • Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95

    Article  Google Scholar 

  • Harborne JB (1997) Role of phenolic secondary metabolites in plants and their degradation in the nature. In: Cadisch G, Giller KE (eds) Driven by nature: Plant litter quality and decomposition. CAB International, Wallingford, pp 67–74

    Google Scholar 

  • Hättenschweiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trend Ecol Evol 15:238–243

    Article  Google Scholar 

  • Haukioja E, Ossipov V, Koricheva J, Honkanen T, Larsson S, Lempa K (1998) Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization? Chemoecology 8:133–139

    Article  CAS  Google Scholar 

  • Havström M, Callaghan TV, Jonasson S (1993) Differential growth responses of Cassiope tetragona, an arctic dwarf-shrub, to environmental perturbations among three contrasting high and sub-arctic sites. Oikos 66:389–402

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869–883

    Article  Google Scholar 

  • IPCC (2001) Third assessment report. Summary for policymakers. A report of working group I of the Intergovernmental Panel on Climate Change. Cambridge Univ Press, Cambridge

  • Jefferies RL, Klein DR, Shaver GR (1994) Herbivores and northern plant communities: reciprocal influences and responses. Oikos 71:193–206

    Article  Google Scholar 

  • Jonasson S, Bryant JP, Chapin FS III, Andersson M (1986) Plant phenols and nutrients in relation to variations in climate and rodent grazing. Am Nat 128:394–408

    Article  CAS  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changed temperature, nutrient and light regimes in the Arctic. Ecology 80:1828–1843

    Article  Google Scholar 

  • Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27–44

    Article  CAS  Google Scholar 

  • Julkunen-Tiitto R, Sorsa S (2001) Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. J Chem Ecol 27:779–789

    Article  PubMed  CAS  Google Scholar 

  • Julkunen-Tiitto R, Rousi M, Bryant JP, Sorsa S, Keinänen M, Sikanen H (1996) Chemical diversity of several Betulaceae species: comparison of phenolics and terpenoids in nothern birch stems. Trees 11:16–22

    Article  Google Scholar 

  • Keinänen M, Julkunen-Tiitto R, Mutikainen P, Walls M, Ovaska J, Vapaavuori E (1999) Trade-offs in phenolic metabolism of silver birch: Effects of fertilization, defoliation, and genotype. Ecology 80:1970–1986

    Google Scholar 

  • Kleiner KV, Raffa KF, Dickson RE (1999) Partitioning of 14 C-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oikos 119:408–418

    Google Scholar 

  • Koricheva J (1999) Interpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations. Oecologia 119:467–473

    Article  Google Scholar 

  • Koricheva J (2002) The carbon-nutrient balance hypothesis is dead; long live the carbon-nutrient balance hypothesis? Oikos 98:537–539

    Article  CAS  Google Scholar 

  • Koricheva J, Larsson S, Haukioja E, Keinänen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos 83:212–226

    Article  CAS  Google Scholar 

  • Kuokkanen K, Julkunen-Tiitto R, Keinänen M, Niemelä P, Tahvanainen J (2001) The effect of elevated CO2 and temperature on the secondary chemistry of Betula pendula seedlings. Trees 15:378–384

    Article  CAS  Google Scholar 

  • Lavola A (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiol 18:53–58

    PubMed  CAS  Google Scholar 

  • Lavola A, Julkunen-Tiitto R (1994) The effect of elevated carbon dioxide and fertilization on primary and secondary metabolites in birch, Betula pendula (Roth). Oecologia 99:315–321

    Article  Google Scholar 

  • Lavola A, Julkunen-Tiitto R, Aphalo P, de la Rosa T M, Lehto T (1997) The effect of UV-B radiation on UV-absorbing secondary metabolites in birch seedlings grown under simulated forest soil conditions. New Phytol 137:617–621

    Article  CAS  Google Scholar 

  • Loomis WE (1932) Growth-differentiation balance vs carbohydrate-nitrogen ratio. Proc Am Soc Hort Sci 29:240–245

    CAS  Google Scholar 

  • Lorio PL (1986) Growth-differentiation balance: a basis for understanding southern pine beetle-tree interactions. For Ecol Manag 14:259–273

    Article  Google Scholar 

  • Michelsen A, Jonasson S, Sleep D, Havström M, Callaghan TV (1996) Shoot biomass, δ13 C, nitrogen and chlorophyll responses of two arctic dwarf shrubs to in situ shading, nutrient application and warming simulating climate change. Oecologia 105:1–12

    Article  Google Scholar 

  • Nadelhoffer KJ, Giblin AE, Shaver GR, Linkins AE (1992) Microbial processes and plant nutrient availability in arctic soils. In: Chapin FS III, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J (eds) Arctic ecosystems in a changing climate. An ecophysiological perspective. Academic Press, San Diego, pp 281–300

    Google Scholar 

  • Peñuelas J, Estiarte M (1998) Can elevated CO2 affect secondary metabolism and ecosystem function? Trend Ecol Evol 13:20–24

    Article  Google Scholar 

  • Reichardt PB, Chapin FS, III Bryant JP, Mattes BR, Clausen TP (1991) Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: Potential importance of metabolite turnover. Oecologia 88:401–406

    Article  Google Scholar 

  • de la Rosa TM, Julkunen-Tiitto R, Lehto T, Aphalo P (2000) Secondary metabolites and nutrient concentrations in silver birch seedlings under five levels of daily UV-B exposure and two relative nutrient addition rates. New Phytol 150:121–131

    Article  Google Scholar 

  • Seigler DS (1998) Tannins. In: Seigler DS (ed) Plant secondary metabolism. Kluwer Acad Publ, Boston, pp 151–192

    Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Statistical Analysis Systems Institute (1999) SAS/STAT Users Guide, Release 8.02. SAS Institute, Cary, NC, USA

  • Tuomi J, Niemelä P, Haukioja E, Sirén S, Neuvonen S (1984) Nutrient stress: an explanation for plant anti-herbivore responses to defoliation. Oecologia 61:208–210

    Article  Google Scholar 

  • Veteli TO, Kuokkanen K, Julkunen-Tiitto R, Roininen, H, Tahvanainen J (2002) Effects of elevated CO2 and temperature on plant growth and herbivore defensive chemistry. Global Ch Biol 8:1240–1252

    Article  Google Scholar 

  • Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific Publications, Oxford, pp 66–103

    Google Scholar 

  • Wood CD, Tiwari BN, Plumb VE, Powell CJ, Roberts BT, Sirimane VDP, Rossiter JT, Gill M (1994) Interspecies differences and variability with time of protein precipitation activity of extractable tannins, crude protein, ash, and dry matter content of leaves from 13 species of Nepalese fodder trees. J Chem Ecol 20:3149–31

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The research was funded by the Danish Natural Science Research Council, the Nordic Council of Minister’s Nordic Arctic Research Programme, the Fiedler scholarship and a scholarship from Abisko Scientific Research Station. Karina E. Clemmensen was kind enough to assist in the fieldwork.

Author information

Authors and Affiliations

  1. Department of Plant Biology, Research Centre Flakkebjerg, 4200, Slagelse, Denmark

    Anja H. Hansen

  2. Department of Terrestrial Ecology, Institute of Biology, University of Copenhagen, Øster Farimagsgade 2D, 1353, Copenhagen K, Denmark

    Sven Jonasson & Anders Michelsen

  3. Natural Product Research Laboratory, Department of Biology, University of Joensuu, P.O. Box 111, FIN, 80101, Joensuu, Finland

    Riitta Julkunen-Tiitto

Authors
  1. Anja H. Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sven Jonasson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anders Michelsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Riitta Julkunen-Tiitto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sven Jonasson.

Additional information

Communicated by Christian Koerner

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hansen, A.H., Jonasson, S., Michelsen, A. et al. Long-term experimental warming, shading and nutrient addition affect the concentration of phenolic compounds in arctic-alpine deciduous and evergreen dwarf shrubs. Oecologia 147, 1–11 (2006). https://doi.org/10.1007/s00442-005-0233-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-005-0233-y

Keywords

Search

Navigation