Summary
Although spinose teeth of holly leaves have been widely cited as an example of a physical defense against herbivores, this assumption is based largely on circumstantial evidence and on general misinterpretation of a single, earlier experiment. We studied the response of third and fifth instar larvae of the fall webworm, Hyphantria cunea Drury, a generalist, edge-feeding caterpillar, to intact American holly leaves and to leaves that had been modified by blunting the spines, by removing sections of leaf margin between the spines, or by removing the entire leaf margin. The results suggest that the thick glabrous cuticle and tough leaf margin of Ilex opaca are more important than the spinose teeth in deterring edge-feeding caterpillars. Microscopic examination of mature leaves revealed that the epidermis is thickened at the leaf margin, and that the leaf is cirucumscribed by a pair of fibrous veins. In simple choice tests neither domesticated rabbits nor captive whitetailed deer discriminated between spinescent holly foliage and foliage from which spines were removed. Nevertheless, we found little evidence of herbivory by mammals in the field, either on small experimental trees or in the forest understory. While it is possible that spinose teeth contribute to defense by reducing acceptibility of holly relative to other palatable plant species, we suggest that the high concentrations of saponins and poor nutritional quality of holly foliage may be more important than spines in deterring vertebrate herbivores. The degree of leaf spinescence and herbivory was compared at different heights with the tree canopy to test the prediction that lower leaves should be more spinescent as a deterrent to browsers. Leaves on lower branches of mature forest trees were slightly more spinescent than were upper leaves, and juvenile trees were slightly more spinescent than were mature trees. However, there was no relationship between degree of spinescence and feeding damage. The greater spinescence of holly leaves low in the canopy is probably an ontogenetic phenomenon rather than a facultative defense against browsers.
Similar content being viewed by others
References
Barber HL (1984) Eastern mixed forest. In: Halls LK (ed) Whitetailed deer: ecology and management. Stackpole Books, Harrisburg, PA, pp 345–354
Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Ann Rev Ecol Syst 13:229–259
Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–233
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899
Cooper SM, Owen-Smith N (1986) Effects of plant spinescence on large mammalian herbivores. Oecologia (Berlin) 68:446–455
Crawley MJ (1983) Herbivory: the dynamics of animal-plant interactions. Blackwell Scientific Publications, Oxford
Edwards PJ, Wratten SD (1980) Ecology of insect-plant interactions. Institute of Biology. Studies in Biology 121. Arnold Publishers, Ltd, London
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:158–608
Ehrlich PR, Raven PH (1967) Butterflies and plants. Sci Amer 216:104–131
Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581
Givnish T (1979) On the adaptive significance of leaf form. In: Solbrig OT, Jain S, Johnson GB, Raven PH (eds) Topics in plant population biology. Columbia Univ Press, New York, pp 375–407
Janzen DH (1980) When is it coevolution? Evolution 34:611–612
Johnson WT, Lyon HH (1976) Insects that feed on trees and shrubs. Cornell Univ Press, Ithaca, NY
Kimmerer TW, Potter DA (1987) Nutritional quality of specific leaf tissues and selective feeding by a specialist leafminer. Oecologia (Berlin) 71:548–551
Kozlowski TT (1971) Growth, and development of trees, vol 1. Academic Press, London
Merz E (1959) Pflanzen und Raupen. Über einige Prinzipien der Futterwahl bei Grosschmetterlingsraupen. Biol Zentr 78:152–188
Mooney HA, Gulmon SL (1982) Constraints on leaf structure and function in relation to herbivory. Bioscience 32:198–206
Peterken GF (1966) Mortality of holly (Ilex aquifolium) seedlings in relation to natural regeneration in the new forest. J Ecol 54:259–269
Potter DA, Kimmerer TW (1986) Seasonal allocation of defense investment in Ilex opaca Aiton and constraints on a specialist leafminer. Oecologia (Berlin) 69:217–224
Raupp MJ, Denno RF (1983) Leaf age as a predictor of herbivore distribution and abundance, pp 91–124. In: Denno RJ, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, NY
Raupp MJ (1985) Effects of leaf toughness on mandibular wear of the leaf beetle, Plagiodera versicolora. Ecol Entomol 10:73–79
Rausher MD (1981) Host plant selection by Battus philenor butterflies: the roles of predation, nutrition, and plant chemistry. Ecol Monogr 51:1–20
Saeki T, Namoto N (1958) On the seasonal change of photosynthetic activity of some deciduous and evergreen broadleaf trees. Bot Mag Tokyo 71:235–241
SAS (1982) General linear models procedure, pp 139–179. In: Statistical analysis system user's guide: statistics. SAS Institute, Inc. Cary, NC
Schaffalitzky de Muckadell M (1954) Juvenile stages in woody plants. Physiol Plantarum 7:782–796
Southwood TRE (1973) The insect/plant relationship — an evolutionary perspective. Symp R Entomol Soc Lond 6:3–30
Supnick M (1983) On the function of leaf spines in Ilex opaca. Bull Torrey Bot Club 110:228–230
Tanton MT (1962) The effects of leaf “toughness” on the feeding of larvae of the mustard beetle. Entomol Exp Appl 5:74–78
Trippi V (1963) Studies on ontogeny and senility in plants. 1. Changes of growth vigor during the juvenile and adult phases of ontogeny in Tilia parviflora, and growth in juvenile and adult zones of Tilia, Ilex aquifolium and Robinia pseudoacacia. Phyton 20:137–145
Walker GP (1985) Stylet penetration by the bayberry whitefly, as affected by leaf age in lemon, Citrus limon. Entomol Exp Appl 39:115–121
Walker GP, Aitken GCD (1985) Oviposition and survival of bayberry whitefly, Parabemisia myricae (Homoptera: Aleyrodidae) on lemons as a function of leaf age. Environ Entomol 14:254–257
Way DW (1956) Some nutrition problems of deer in the southern pine type. Proc SE Assoc Game and Fish Comm 10:53–58
Williams LH (1954) The feeding habits and food preference of Acrididae and the factors which determine them. Trans R Entomol Soc Lond 105:423–454
Author information
Authors and Affiliations
Additional information
The investigation reported in this paper (No. 87-7-8-77) is in connection with a project of the Kentucky Agricultural Experiment Station and is published with the approval of the Dirctor
Rights and permissions
About this article
Cite this article
Potter, D.A., Kimmerer, T.W. Do holly leaf spines really deter herbivory?. Oecologia 75, 216–221 (1988). https://doi.org/10.1007/BF00378601
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00378601