Herbivore damage, resource richness and putative defences in juvenile versus adult Eucalyptus leaves
Emma K. Gras A , Jennifer Read A C , Chantal T. Mach A B , Gordon D. Sanson A and Fiona J. Clissold AA School of Biological Sciences, Monash University, Vic. 3800, Australia.
B Université Pierre et Marie Curie Paris VI, France.
C Corresponding author. Email: jenny.read@sci.monash.edu.au
Australian Journal of Botany 53(1) 33-44 https://doi.org/10.1071/BT04049
Submitted: 30 March 2004 Accepted: 7 October 2004 Published: 18 February 2005
Abstract
Eucalyptus species often show marked differences in morphology and ecophysiology between adult and juvenile leaves. Given these differences, it was hypothesised that juvenile and adult leaves would present different levels of resources to a herbivore, and potentially different levels of putative anti-herbivore defences. This hypothesis was tested in some eucalypts growing in native forest in south-eastern Australia.
There were no significant differences in levels of water, protein or carbohydrates (per unit dry weight) between mature adult and juvenile leaves. No difference was recorded in concentration of total phenolics between leaf forms, but more protein was precipitated (an estimate of tannin activity) in extracts from juvenile leaves. Cyanogenic glycosides were absent from mature leaves, but present in young leaves of both leaf forms in E. polyanthemos. No significant difference in concentration of any terpene was recorded between adult and juvenile leaves in E. nitens and E. regnans. Specific leaf area was lower in adult leaves, and fibre concentration was higher in adult leaves of some species, suggesting that resources in the adult leaf may be less accessible to a herbivore. However, there was no difference in leaf toughness between leaf forms, even though toughness per unit leaf thickness was higher in juvenile leaves. Hence, no major trends in resource concentration were apparent between the leaf forms, and of the defences investigated, only tannin activity varied significantly between the leaf forms.
Acknowledgments
We thank Peter West and Scott Metcalf of Forestry Victoria (Department of Sustainability and Environment (DSE)) for advice on locations of species, and for facilitating access to areas of the Tanjil State Forest, and DSE for permission to collect native flora. We thank Tony Patti, Peter Neville-Jones and John Beardall for advice on analysis of terpenes, and John Beardall for use of his GCMS.
Ashton DH, Turner JS
(1979) Studies on the light compensation point of Eucalyptus regnans F.Muell. Australian Journal of Botany 27, 589–607.
Asquith TN, Butler LG
(1985) Use of dye-labeled protein as spectrophotometric assay for protein precipitants such as tannin. Journal of Chemical Ecology 11, 1535–1544.
| Crossref |
Ball S
(1994) A comparison of leaf structure in deciduous and evergreen species of Nothofagus. BSc (Hons) Thesis
(Monash University:
Australia)
Beadle CL,
McLeod DE,
Turnbull CRA,
Ratkowsky DA, McLeod R
(1989) Juvenile/total foliage ratios in Eucalyptus nitens and the growth of stands and individual trees. Trees 3, 117–124.
| Crossref |
Bell, DT ,
and
Williams, JE (1997). Eucalypt ecophysiology. In ‘Eucalypt ecology: individuals to ecosystems’. pp. 168–196. (Cambridge University Press: Cambridge)
Blackburn DT
(1978) A colorfast stain for polyester-embedded ligneous tissues. Stain Technology 53, 356–358.
Bradford MM
(1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| PubMed |
Brennan EB, Weinbaum SA
(2001) Performance of adult psyllids in no-choice experiments on juvenile and adult leaves of Eucalyptus globulus. Entomologia Experimentalis et Applicata 100, 179–185.
Cameron RJ
(1970) Light intensity and the growth of Eucalyptus seedlings. I. Ontogenetic variation in E. fastigata. Australian Journal of Botany 18, 29–43.
Chabot BF, Hicks DJ
(1982) The ecology of leaf life spans. Annual Review of Ecology and Systematics 13, 229–259.
| Crossref | GoogleScholarGoogle Scholar |
Choong MF
(1996) What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars. Functional Ecology 10, 668–674.
Coley PD
(1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53, 209–233.
Coley PD
(1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74, 531–536.
| Crossref | GoogleScholarGoogle Scholar |
Coley, PD ,
and
Aide, TM (1991). Comparisons of herbivory and plant defenses in temperate and tropical broad-leaved forests. In ‘Plant–animal interactions: evolutionary ecology in tropical and temperate regions’. pp. 25–49. (John Wiley and Sons Inc.: New York)
Coley PD,
Bryant JP, Chapin FS
(1985) Resource availability and plant antiherbivore defense. Science 230, 895–899.
Cork SJ, Krockenberger AK
(1991) Methods and pitfalls of extracting condensed tannins and other phenolics from plants: Insights from investigations on Eucalyptus leaves. Journal of Chemical Ecology 17, 123–134.
| Crossref |
Costermans, L (1983). ‘Native trees and shrubs of south-eastern Australia.’ (Weldon Publishing: Sydney)
Dubois M,
Gilles KA,
Hamilton JK,
Rebers PA, Smith F
(1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
Dungey HS,
Potts BM,
Carnegie AJ, Ades PK
(1997) Mycosphaerella leaf disease: genetic variation in damage to Eucalyptus nitens, Eucalyptus globulus and their F1 hybrid. Canadian Journal of Forest Research 27, 750–759.
| Crossref | GoogleScholarGoogle Scholar |
Edwards PB
(1982) Do waxes on juvenile Eucalyptus leaves provide protection from grazing insects? Australian Journal of Ecology 7, 347–352.
Edwards PB,
Wanjura WJ, Brown WV
(1993) Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids. Oecologia 95, 551–557.
Farrow, RA (1993). Chemical defenses in eucalypts and how they can be exploited to reduce insect attack. In ‘Pest control and sustainable agriculture’. pp. 313–316. (CSIRO: Melbourne)
Farrow RA,
Floyd RB, Newmann FG
(1994) Inter-provenance variation in resistance of Eucalyptus globulus juvenile foliage to insect feeding. Australian Forestry 57, 65–68.
Fox LR, Macauley BJ
(1977) Insect grazing on Eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia 29, 145–162.
Givnish TJ
(1988) Adaptation to sun and shade: a whole plant perspective. Australian Journal of Plant Physiology 15, 63–92.
Graham HD
(1992) Stabilization of the prussian blue color in the determination of polyphenols. Journal of Agricultural and Food Chemistry 40, 801–805.
Hagerman AE,
Riedl KM,
Jones GA,
Sovik KN,
Ritchard NT,
Hartzfeld PW, Riechel TL
(1998) High molecular weight plant polyphenolics (tannins) as biological antioxidants. Journal of Agricultural and Food Chemistry 46, 1887–1892.
| Crossref | GoogleScholarGoogle Scholar |
Harborne, JB (1984). ‘Phytochemical methods: a guide to modern techniques of plant analysis.’ 2nd edn. (Chapman and Hall: London)
Harborne, JB (1991). Recent advances in the ecological chemistry of plant terpenoids. In ‘Ecological chemistry and biochemistry of plant terpenoids’. pp. 399–426. (Oxford University Press: Oxford)
Harborne, JB (1993). ‘Introduction to ecological biochemistry.’ 4th edn. (Academic Press: London)
Heatwole H,
Lowman MD,
Donovan C, McCoy M
(1997) Phenology of leaf-flushing and macroarthropod abundances in canopies of Eucalyptus saplings. Selbyana 18, 200–214.
Heatwole H,
Lowman MD, Abbott KL
(1999) Grazing on Australian eucalypt leaves by insects. Selbyana 20, 299–323.
Howlett BG,
Clarke AR, Madden JL
(2001) The influence of leaf age on the oviposition preference of Chrysophtharta bimaculata (Olivier) and the establishment of neonates. Agricultural and Forest Entomology 3, 121–127.
| Crossref | GoogleScholarGoogle Scholar |
James SA, Bell DT
(2001) Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus ssp. globulus (Myrtaceae). Australian Journal of Botany 49, 259–269.
| Crossref | GoogleScholarGoogle Scholar |
James SA,
Smith WK, Vogelmann TC
(1999) Ontogenetic differences in mesophyll structure and chlorophyll distribution in Eucalyptus globulus ssp. globulus (Myrtaceae). American Journal of Botany 86, 198–207.
Jeanes, JA (1996). Myrtaceae. In ‘Flora of Victoria. Vol. III’. pp. 942–1044. (Inkata Press: Melbourne)
Johnson ED
(1926) A comparison of the juvenile and adult leaves of Eucalyptus globulus. New Phytologist 26, 202–212.
Jones CS
(1995) Does shade prolong juvenile development? A morphological analysis of leaf shape changes in Cucurbita argyrosperma subsp. sororia (Cucurbitaceae). American Journal of Botany 82, 346–359.
Jordan GJ,
Potts BM,
Chalmers P, Wiltshire RJE
(2000) Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp. globulus is an adaptive trait. Australian Journal of Botany 48, 561–567.
Landsberg J
(1989) A comparison of methods for assessing defoliation, tested on eucalypt trees. Australian Journal of Ecology 14, 423–440.
Lee BH,
Choi WS,
Lee SE, Park BS
(2001) Fumigant toxicity of essential oils and their constituent compounds towards the rice weevil, Sitophilus oryzae. Crop Protection 20, 317–320.
| Crossref | GoogleScholarGoogle Scholar |
Li H,
Madden JL, Potts BM
(1995) Variation in volatile leaf oils of the Tasmanian Eucalyptus species. I. Subgenus Monocalyptus. Biochemical Systematics and Ecology 23, 299–318.
| Crossref | GoogleScholarGoogle Scholar |
Li H,
Madden JL, Potts BM
(1996) Variation in volatile leaf oils of the Tasmanian Eucalyptus species. II. Subgenus Symphyomyrtus. Biochemical Systematics and Ecology 24, 547–569.
| Crossref | GoogleScholarGoogle Scholar |
Lowman MD, Heatwole H
(1992) Spatial and temporal variability in defoliation of Australian eucalypts. Ecology 73, 129–142.
Lowry B,
Lee D, Hebant C
(1980) The origin of land plants: a new look at an old problem. Taxon 29, 183–197.
McKey, DD (1979). The distribution of secondary compounds within plants. In ‘Herbivores: their interactions with secondary plant metabolites’. pp. 55–133. (Academic Press: New York)
McLean S,
Foley WJ,
Davies NW,
Brandon S,
Duo L, Blackman AJ
(1993) Metabolic fate of dietary terpenes from Eucalyptus radiata in common ringtail possum (Pseudocheirus peregrinus). Journal of Chemical Ecology 19, 1625–1643.
| Crossref |
Mount AB
(1979) Natural regeneration processes in Tasmanian forests. Search 10, 180–186.
Ohmart CP, Edwards PB
(1991) Insect herbivory on Eucalyptus. Annual Review of Entomology 36, 637–657.
| Crossref | GoogleScholarGoogle Scholar |
Pederick LA
(1979) Natural variation in shining-gum (Eucalyptus nitens). Australian Forest Research 9, 41–63.
Potts, BM ,
and
Jackson, WD (1986). Evolutionary processes in the Tasmanian high altitude eucalypts. In ‘Flora and fauna of alpine Australasia: ages and origins’. pp. 511–527. (CSIRO: Melbourne)
Price ML, Butler LG
(1977) Rapid visual estimation and spectrophotometric determination of tannin content of sorghum grain. Journal of Agricultural and Food Chemistry 25, 1268–1273.
Pryor, LD (1976). ‘The biology of eucalypts.’ (Edward Arnold: London)
Read J, Sanson GD
(2003) Characterising sclerophylly: the mechanical properties of a diverse range of leaf types. New Phytologist 160, 81–99.
| Crossref | GoogleScholarGoogle Scholar |
Read J,
Edwards C,
Sanson GD, Aranwela N
(2000) Relationships between sclerophylly, leaf biomechanical properties and leaf anatomy in some Australian heath and forest species. Plant Biosystems 134, 261–277.
Read J,
Gras E,
Sanson GD,
Clissold F, Brunt C
(2003) Does chemical defence decline more in developing leaves that become strong and tough at maturity? Australian Journal of Botany 51, 489–496.
| Crossref | GoogleScholarGoogle Scholar |
Sanson GD,
Stolk R, Downes BJ
(1995) A new method for characterizing surface roughness and available space in biological systems. Functional Ecology 9, 127–135.
Sanson G,
Read J,
Aranwela N,
Clissold F, Peeters P
(2001) Measurement of leaf biomechanical properties in studies of herbivory: opportunities, problems and procedures. Austral Ecology 26, 535–546.
| Crossref | GoogleScholarGoogle Scholar |
Smith D,
Paulsen GM, Raguse CA
(1964) Extraction of total available carbohydrates from grass and legume tissue. Plant Physiology 39, 960–962.
Thomas DA, Barber HN
(1974) Studies on leaf characteristics of a cline of Eucalyptus urnigera from Mount Wellington, Tasmania. II. Water repellency and the freezing of leaves. Australian Journal of Botany 22, 501–512.
Timmins WA,
Bellward K,
Stamp AJ, Reynolds SE
(1988) Food intake, conversion efficiency, and feeding behaviour of tobacco hornworm caterpillars given artificial diet of varying nutrient and water content. Physiological Entomology 13, 303–314.
Van Soest PJ,
Robertson JB, Lewis BA
(1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
| PubMed |
Wiltshire RJE,
Potts BM, Reid JB
(1991) A paedomorphocline in Eucalyptus: natural variation in the E. risdonii/E. tenuiramis complex. Australian Journal of Botany 39, 545–566.