Skip to main content
SpringerLink
Log in

Growth cost and ontogenetic expression patterns of defence in cyanogenic Eucalyptus spp.

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Plant defences can incur allocation costs and such costs incurred early in ontogeny may result in opportunity costs with effects evident later in life. A unified understanding of the growth cost of defence requires the identification of plants with varying ontogenetic trajectories of preferably resource demanding defences and an appropriate measurement of the growth cost of these defences. To develop such tools, we first compared nitrogen-based chemical defence (cyanogenic glycosides) in juvenile and adult foliage of three species of Eucalyptus (Myrtaceae). We found marked differences between the species, with two having much lower concentrations of foliar cyanogenic glycosides in seedlings compared to adults. We next used seedlings of two species to measure the resource (nitrogen) and growth cost of deploying cyanogenic glycosides. We found evidence that for every 1.0 nitrogen invested in cyanogenic glycosides, 1.49 additional nitrogens were effectively added to the leaves. We also found that deployment of cyanogenic glycosides was associated with a reduction in net assimilation rate (NAR) at constant leaf nitrogen. We did not, however, detect an overall growth cost associated with cyanogenic glycoside deployment because the rise in leaf nitrogen associated with this deployment apparently counteracted the reduction in NAR.

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

Similar content being viewed by others

Abbreviations

CNA :

Leaf cyanide per unit leaf area

CNm :

Leaf cyanide per unit leaf mass

CN-N/N:

Cyanide–nitrogen as a proportion of total leaf nitrogen

Ec :

Eucalyptus cladocalyx

Ep :

E. polyanthemos

Ey :

E. yarraensis

LAR:

Leaf area ratio

LMA:

Leaf mass per unit leaf area

LL:

Leaf longevity

LNP:

Leaf nitrogen productivity

LWR:

Leaf weight ratio

NA :

Total leaf nitrogen per unit leaf area

NAR:

Net assimilation rate

NCN-A :

Nitrogen in cyanide on a leaf area basis

NM :

Total leaf nitrogen per unit leaf mass

RGR:

Relative growth rate

SLA:

Specific leaf area

References

  • Ashton DH (2000) Ecology of eucalypt regeneration. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of eucalypts. CSIRO, Melbourne, pp 47–60

    Google Scholar 

  • Berenbaum MR (1995) Turnabout is fair play: secondary roles for primary compounds. J Chem Ecol 21:925–940

    Article  CAS  Google Scholar 

  • Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558

    Article  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Brinker AM, Seigler DS (1989) Methods for the detection and quantitative determination of cyanide in plant materials. Phytochem Bull 21:24–31

    Google Scholar 

  • Bryant JP, Reichart PB, Clausen TP, Provenza FO, Kuropat PJ (1992) Woody plant–mammal interactions. In: Rosenthal GA, Berenbaum MR (eds) Herbivores. Their interactions with secondary plant metabolites. Academic Press, New York, pp 343–370

    Google Scholar 

  • Burns A, Gleadow RM, Woodrow IE (2002) Light alters the allocation of nitrogen to cyanogenic glycosides in Eucalyptus cladocalyx. Oecologia 133:288–294

    Article  Google Scholar 

  • Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233

    Article  Google Scholar 

  • Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Cork SJ, Krockenburger AK (1991) Methods and pitfalls of extracting condensed tannins and other phenolics from plants: insights from investigations on Eucalyptus leaves. J Chem Ecol 17:123–134

    Article  CAS  Google Scholar 

  • Dahler JM, McConchie CA, Turnbull CGN (1995) Quantification of cyanogenic glycosides in seedlings of three Macadamia (Proteaceae) species. Aust J Bot 43:619–628

    Article  CAS  Google Scholar 

  • de Boer NJ (1999) Pyrrolizidine alkaloid distribution in Senecio jacobaea rosettes minimises losses to generalist feeding. Entomol Exp Appl 91:169–173

    Article  CAS  Google Scholar 

  • de Jung TJ (1995) Why fast-growing plants do not bother about defense. Oikos 74:545–548

    Article  Google Scholar 

  • Diemer M (1998) Life span and dynamics of leaves of herbaceous perennials in high-elevation environments: ‘news from the elephant's leg’. Funct Ecol 12:413–425

    Article  Google Scholar 

  • Gill AM (1993) Interplay of Victoria's flora with fire. In: Foreman DB, Walsh NG (eds) Flora of Victoria, vol 1, Introduction. Inkata Press, Melbourne, pp 212–226

    Google Scholar 

  • Gleadow RM (1999) Resource allocation in Eucalyptus cladocalyx. PhD thesis, School of Botany, University of Melbourne, Melbourne

  • Gleadow RM, Woodrow IE (2002a) Constraints on effectiveness of cyanogenic glycosides in herbivore defense. J Chem Ecol 28:1297–1309

    Article  Google Scholar 

  • Gleadow RM, Woodrow IE (2002b) Defence chemistry of cyanogenic Eucalyptus cladocalyx seedlings is affected by water supply. Tree Physiol 22:939–945

    PubMed  CAS  Google Scholar 

  • Gleadow RM, Foley WJ, Woodrow IE (1998) Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell. Plant, Cell Environ 21:12–22

    Article  CAS  Google Scholar 

  • Goodger JQD (2002) Characterising the polymorphism for cyanogenesis in Eucalyptus. PhD thesis, University of Melbourne, Melbourne

  • Goodger JQD, Woodrow IE (2002) Cyanogenic polymorphism as an indicator of genetic diversity in the rare species Eucalyptus yarraensis (Myrtaceae). Funct Plant Biol 29:1445–1452

    Article  CAS  Google Scholar 

  • Goodger JQD, Capon RJ, Woodrow IE (2002) Cyanogenic polymorphism in Eucalyptus polyanthemos Schauer subsp. vestita L. Johnson and K. Hill (Myrtaceae). Biochem Syst Ecol 30:617–630

    Article  CAS  Google Scholar 

  • Goodger JQD, Ades PK, Woodrow IE (2004) Cyanogenesis in Eucalyptus polyanthemos seedlings: heritability, ontogeny and effect of soil nitrogen. Tree Physiol 24:681–688

    PubMed  Google Scholar 

  • Grime JP, Hunt R (1975) Relative growth-rate: its range and adaptive significance in a local flora. J Ecol 63:393–422

    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 

  • Hooda N, Weston CJ (1999) The effects of site and fertilizer addition on foliage and litter quality in six-year-old Eucalyptus globulus (Labill.) plantations in Gippsland, southeastern Australia. Aust J Bot 47:189–206

    Article  Google Scholar 

  • Huntly NJ (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503

    Article  Google Scholar 

  • Julkunen-Tiitto R, Bryant JP, Kuropat P, Roininen H (1995) Slight tissue wounding fails to induce consistent chemical defense in three willow (Salix spp.) clones. Oecologia 101:467–471

    Article  Google Scholar 

  • Kakes P (1989) An analysis of the costs and benefits of the cyanogenic system in Trifolium repens L. Theor Appl Genet 77:111–118

    Article  Google Scholar 

  • Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190

    Google Scholar 

  • Kouki M, Manetas Y (2002) Toughness is less important than chemical composition of Arbutus leaves in food selection by Poecilimon species. New Phytol 154:399–407

    Article  CAS  Google Scholar 

  • Kriedemann PE, Cromer RN (1996) The nutritional physiology of the Eucalypts—nutrition and growth. In: Attiwill PM, Adams MA (eds) Nutrition of the Eucalypts. CSIRO, Melbourne, pp 109–122

    Google Scholar 

  • Lambdon PW, Hassall M, Boar RR, Mithen R (2003) Asynchrony in the nitrogen and glucosinolate leaf-age profiles of Brassica: is this a defensive strategy against generalist herbivores? Agric Ecosyst Environ 97:205–214

    Article  CAS  Google Scholar 

  • Landsberg JJ, Cork SJ (1997) Herbivory: interactions between eucalypts and the vertebrates and invertebrates that feed on them. In: Williams JE, Woinarski JCZ (eds) Eucalypt ecology. Cambridge University Press, Cambridge, UK, pp 342–372

    Google Scholar 

  • Lawler IR, Foley WJ, Woodrow IE, Cork SJ (1997) The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109:59–68

    Article  Google Scholar 

  • Lawrence R, Potts BM, Whitham TG (2003) Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84:1171–1178

    Google Scholar 

  • McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320

    Article  Google Scholar 

  • Miller RE, Gleadow RM, Woodrow IE (2004) Cyanogenesis in tropical Prunus turneriana: characterisation, variation and response to low light. Funct Plant Biol 31:491–503

    Article  Google Scholar 

  • Mooney HA, Gulmon SL (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32:198–206

    Article  CAS  Google Scholar 

  • Nahrstedt A (1985) Cyanogenic compounds as protecting agents for organisms. Plant Syst Evol 150:35–47

    Article  CAS  Google Scholar 

  • Neilson EH, Goodger JQD, Woodrow IE (2006) Novel aspects of cyanogenesis in Eucalyptus camphora subsp. humeana. Funct Plant Biol 33:487–496

    Article  CAS  Google Scholar 

  • Ohnmeiss TE, Baldwin IT (2000) Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 81:1765–1783

    Article  Google Scholar 

  • Reich PB, Walkers MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  PubMed  CAS  Google Scholar 

  • Ryser P, Urbas P (2000) Ecological significance of leaf life span among Central European grass species. Oikos 91:41–50

    Article  Google Scholar 

  • Sagers C, Coley PD (1995) Benefits and costs of defense in a neotropical shrub. Ecology 76:1835–1843

    Article  Google Scholar 

  • Schappert PJ, Shore JS (2000) Cyanogenesis in Turnera ulmifolia L (Turneraceae): II. Developmental expression, heritability and cost of cyanogenesis. Evol Ecol Res 2:337–352

    Google Scholar 

  • Selmar D, Grocholewski S, Seigler DS (1990) Cyanogenic lipids: utilization during seedling development of Ungnadia speciosa. Plant Physiol 93:631–636

    Article  PubMed  CAS  Google Scholar 

  • Selmar D, Lieberei R, Junqueira NTV, Biehl B (1991) Changes in cyanogenic glucoside content in seeds and seedlings of Hevea species. Phytochemistry 30:2135–2140

    Article  CAS  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–284

    Article  Google Scholar 

  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77

    Article  PubMed  CAS  Google Scholar 

  • Tilman D (1990) Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos 58:3–15

    Article  Google Scholar 

  • Wallace SK, Eigenbrode SD (2002) Changes in the glucosinolate–myrosinase defense system in Brassica juncea cotyledons during seedling development. J Chem Ecol 28:243–256

    Article  PubMed  CAS  Google Scholar 

  • Wellington AB (1989) Seedling regeneration and population dynamics of eucalypts. In: Noble JC, Bradstock RA (eds) Mediterranean landscapes in Australia. CSIRO, Melbourne, pp 155–167

    Google Scholar 

  • Woodrow IE, Slocum DJ, Gleadow RM (2002) Influence of water stress on cyanogenic capacity in Eucalyptus cladocalyx. Funct Plant Biol 29:103–110

    Article  CAS  Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Baldwin IT (2004) Constitutive and inducible trypsin protease inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Natl Acad Sci USA 101:1607–1612

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. Barry Smith of the Glenville Stud, South Australia, for access to trees on private land. The Department of Natural Resources and Environment, Victoria, provided permits to take protected flora (#10001252) and for fieldwork in Brisbane Ranges National Park, Victoria (#10000781). This research was supported by funds from an Australian Research Council Grant to IEW and in part by the Holsworth Wildlife Research Fund (Victorian Community Foundation, ANZ Charitable Trusts). JQDG was a recipient of an Australian Postgraduate Award Scholarship.

Author information

Author notes

  1. Roslyn M. Gleadow

    Present address: School of Biological Sciences, Monash University, Victoria, 3800, Australia

Authors and Affiliations

  1. School of Botany, University of Melbourne, Victoria, 3010, Australia

    Jason Q. D. Goodger, Roslyn M. Gleadow & Ian E. Woodrow

Authors
  1. Jason Q. D. Goodger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roslyn M. Gleadow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ian E. Woodrow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jason Q. D. Goodger.

Additional information

Communicated by M. Adams

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goodger, J.Q.D., Gleadow, R.M. & Woodrow, I.E. Growth cost and ontogenetic expression patterns of defence in cyanogenic Eucalyptus spp.. Trees 20, 757–765 (2006). https://doi.org/10.1007/s00468-006-0090-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-006-0090-2

Keywords

Search

Navigation