Oecologia

, Volume 71, Issue 2, pp 254–261

Interactions between oak tannins and parasite community structure: Unexpected benefits of tannins to cynipid gall-wasps

  • M. L. Taper
  • T. J. Case
Original Papers

Abstract

Plant species vary tremendously in the number of phytophagous species they support. May (1979) and Price (1980) proposed that some of this variation may be due to variation in biochemical defenses. We find that variation between oak species in leaf tannin levels is positively correlated with 1) variation in the numbers of species of leaf-galling cynipid wasps those trees host; and 2) the density of individual galls per oak leaf. We hypothesize that leaf and gall tannins serve a protective function for cynipids, decreasing the amount of cynipid larval mortality due to fungal infestation. This defensive function would explain the observed positive relationships between oak tannin levels and cynipid diversity as well as cynipid abundance.

Key words

Oak Cynipid gall-wasps Species number Tannin 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Askew RR (1980) Polyphagus/specific parasites of cynipids. J Anim Ecol 49:817–829Google Scholar
  2. Bate-Smith EC (1973a) Haemanalysis of tannins: the concept of relative astringency. Phytochemistry 12:907–912Google Scholar
  3. Bate-Smith EC (1973b) Tannins of the herbaceous Leguminosae. Phytochemistry 12:1809–1812Google Scholar
  4. Bate-Smith EC (1977) Astringent tannins of Acer species. Phytochemistry 16:1421–1426Google Scholar
  5. Belserene R (1980) Leaf Tannins 1) factors affecting leaf astringency and 2) developmental changes in leaf tannins and nitrogen in Quercus wislizenii and Arbutus menzeisi. Master's Thesis, University of California, Santa CruzGoogle Scholar
  6. Berenbaum M (1980) Adaptive significance of midgut pH in larval Lepidoptera. Am Nat 115:138–146Google Scholar
  7. Berenbaum M (1981) Patterns of furanocoumarin distribution and insect herbivory in the Umbelliferae: Plant chemistry and community structure. Ecology 62(5):1254–1266Google Scholar
  8. Berenbaum M (1983) Coumarins and caterpillars — A case for coevolution. Evolution 37:163–179Google Scholar
  9. Bernays EA (1978) Tannins: an alternative viewpoint. Ent Exp Appl 24:44–53Google Scholar
  10. Bernau EA, Woodhead S (1982) Plant phenols utilized as nutrients by a phytophagous insect. Science 216:201–202Google Scholar
  11. Burnett JA (1974) A new cynipid wasp from California. Pan Pac Entomol 50:298–302Google Scholar
  12. Burnett JA (1977) Biosystematics of the new oak-gall wasp genus, Weldia, of western North America (Hymenoptera: Cynipidae). Ph D Thesis, University of California, RiversideGoogle Scholar
  13. Carroll CR, Hoffman CA (1980) Chemical feeding deterrent mobilized in response to insect herbivory and counteradaptation by Epilachna tredecinata. Science 209:414–416Google Scholar
  14. Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipidae (Hymenoptera): why and how? Am Midl Nat 110:225–234Google Scholar
  15. Cornell HV (1985) Local and regional richness of cynipine galls wasps on California oaks. Ecology 66:1247–1260Google Scholar
  16. Cornell HV, Washburn JO (1979) Evolution of the richness-area correlation for cynipid gall-wasps on oak trees: a comparison of two geographic areas. Evolution 33:257–274Google Scholar
  17. Cruickshank IAM (1980) Defenses triggered by the invader: chemical defenses. In Plant Disease (Horsfall, JG and Cowling EB, editors), Vol 5, Academic Press, New York pp 247–267Google Scholar
  18. Doutt RL (1959) Heterogony in Dryocosmus Hymenoptera Cynipidae. Ann Ent Soc Amer 52:69–74Google Scholar
  19. Ehrlich PR, Raven PH (1964) Butterflies and plants: A study in coevolution. Evol 18:586–608Google Scholar
  20. Edmunds GF Jr, Alstad DN (1978) Coevolution in insect herbivores and conifers. Science 199:941–945Google Scholar
  21. Edwards PJ, Wratten, SD, Greenwood S (1986) Palatability of British trees to insects: constitutive and induced defenses. Oecologia 69:316–319Google Scholar
  22. Faeth SH (1985) Host leaf selection by leaf miners: interaction among three trophic levels. Ecology 66(3):870–875Google Scholar
  23. Faeth SH (1986) Indirect interaction between temporally-separated herbivores mediated by the host plant. Ecology (in press)Google Scholar
  24. Faeth SH, Bultman TL (1986) Interacting effects of increased tannin levels on leaf-mining insects. Entomol Exper Appl (in press)Google Scholar
  25. Feeny PP (1968) Effect of oak leaf tannins on larval growth of the Winter moth Operaphtera brunata. J Insect Physiol 14:805–817Google Scholar
  26. Feeny P (1969) Inhibitory effect of oak leaf tannins on the hydrolysis of proteins by trypsin. Phytochemistry 8:2119–2126Google Scholar
  27. Feeny PP (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by Winter moth caterpillars. Ecology 51:565–581Google Scholar
  28. Feeny PP (1975) Biochemical coevolution between plants and their herbivores. In: Coevolution of animals and plants. Eds LE Gilbert and PH Raven., University of Texas Press, Austin pp 3–19Google Scholar
  29. Feeny PP (1976) Plant apparency and chemical defense. Rec Adv Phytochemistry 10:1–40Google Scholar
  30. Felt EP (1940) Plant galls and gall makers. The Comstock Publ Co, Ithaca, New YorkGoogle Scholar
  31. Fox LR, Macauley BJ (1977) Insect grazing on eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia (Berlin) 29:145–162Google Scholar
  32. Gilbert LE (1971) Butterfly-plant coevolution: has Passiflora adenopoda won the selection race with heliconine butterflies? Science 172:585–586Google Scholar
  33. Gilbert LE (1975) Ecological consequences of a coevolved mutualism between butterflies and plants. In: Coevolution of animals and plants. Eds Gilbert LE, Raven PH (eds) University of Texas Press, Austin pp 210–240Google Scholar
  34. Goldstein JL, Swain T (1965) The inhibition of enzymes by tannins. Phytochemistry 4:185–192Google Scholar
  35. Goodman D (1986) Considerations of stochastic demography in the design and management of reserves. Natural Resource Modeling (in press)Google Scholar
  36. Harborne JB, Ingham JL (1978) Biochemical aspects of the coevolution of higher plants with their fungal parasites. In: Biochemical Aspects of Plant and Animal Coevolution Harborne JB (ed), Academic Press, New York pp 343–405Google Scholar
  37. Hendrix SB (1980) An evolutionary and ecological perspective of the insect fauna of ferns. Amer Nat 115:171–196Google Scholar
  38. Howes FN (1953) Vegetable tanning materials. Butterworth, LondonGoogle Scholar
  39. Jones DA (1962) Selective eating of the acyanogenic form of the plant Lotus corniculatu by various animals. Nature 193:1109–1110Google Scholar
  40. Jones DA (1972) Cyanogenic glycosides and their function. In: Phytochemical ecology. Harborne JB (ed) Academic Press, New YorkGoogle Scholar
  41. Karban R, Ricklefs RE (1984) Leaf traits and species richness and abundance of lepidopteran larvae on deciduous trees in southern Ontario. Oikos 43:165–170Google Scholar
  42. Larew HG (1982) A comparative anatomical study of galls caused by the major cecidogenetic groups with special emphasis on the nutritive tissue Ph D Dissertation, Oregon State UniversityGoogle Scholar
  43. Leight EG (1981) The average lifetime of a population in a varying environment. J Theor Biol 90:213–239Google Scholar
  44. Li HL, Hsiao JY (1974) A preliminary study of the chemosystematics of American oaks: phenolic characters of leaves. Bartonia 42:5–13Google Scholar
  45. Little EL (1971) Atlas of United States trees. Vol I, 8 pp, 200 maps USDA Forest Service Misc Publ 1146Google Scholar
  46. Little EL (1976) Atlas of United States trees. Minor western hardwoods. Vol 3, 13 pp, 290 maps USDA Forest Service Misc Publ 1314Google Scholar
  47. Lyon RL (1959) An alternating sexual generation in the gall wasp, Callirhytis pomiformis. Bull So Calif Acad of Sci 58:33–37Google Scholar
  48. Lyon RL (1963) An alternate generation of Heteroecus pacificus. Proc Ento Soc Wash 65:250–254Google Scholar
  49. Lyon RL (1969) The alternate generation of Callirhytis quercussuttoni. Proc Ento Soc Wash 71:61–65Google Scholar
  50. MacArthur RH (1972) Geographical ecology. Harper and Row, New YorkGoogle Scholar
  51. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, NJGoogle Scholar
  52. May RM (1979) Patterns in the abundance of parasites on plants. Nature 281:425–426Google Scholar
  53. Morrow PA, Fox LR (1980) Effects of variation in eucalyptus essential oil yield on insect growth and grazing damage. Oecologia (Berlin) 45:209–219Google Scholar
  54. Parker J (1977) Phenolics in black oak bark and leaves. J Chem Ecol 3:489–496Google Scholar
  55. Price P (1980) Evolutionary biology of parasites. Princeton Monographs in Population Biology. Princeton University Press, Princeton, NJGoogle Scholar
  56. Reese JC (1978) Chronic effects of plant allelochemics on insect nutritional physiology. Ent Exp Appl 24:425–431Google Scholar
  57. Rhoades DH, Cates RG (1976) Towards a general theory of plant antiherbivore chemistry. Recent Advances in Phytochem 10:168–213Google Scholar
  58. Roeske CN, Seiber JN, Brower LB, Moffit CM (1976) Milkweed cardenolides and their comparative processing by monarch butterflies. Recent Advances in Phytochem 10:93–167Google Scholar
  59. Rowell-Rahier M (1984) The presence or absence of phenylagrosides in Salix (Salicacene) leaves and the level of dietary specialisation of some of their herbivorous insects. Oecologia (Berlin) 62:26–30Google Scholar
  60. Schoonhoven LM, Meerman J (1978) Metabolic costs of changes in diet and neutralization of allelochemics. Ent Exp Appl 24:489–493Google Scholar
  61. Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–150Google Scholar
  62. Sen Gupta GC, Miles PW (1975) Studies on the susceptibility of varieties of apple to the feeding of two strains of woolly aphids (Homoptera) in relation to the chemical content of the tissues of the host. Aust J Agr Res 26:127–136Google Scholar
  63. Smiley JT, Horn JM, Rank NE (1985) Ecological effects of salicin at three trophic levels: new problems from old adaptations. Science 229:649–651Google Scholar
  64. Sørenson T (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species content. Kong Dan Vidensk Selsk Biol Skr 5:1–34Google Scholar
  65. Swain T (1979) Tannins and lignins. In: Herbivores: Their interactions with secondary plant metabolites. Eds Rosenthal GA, Janzen D (eds). Academic Press, New York, pp 657–682Google Scholar
  66. Taper ML, Zimmerman EM, Case TJ (1986) Sources of mortality for a cynipid gall-wasp (Dryocosmus dubiosus (Hymenoptera: Cynipidae)): The importance of the tannin/fungus interaction. Oecologia (Berlin) 68:437–495Google Scholar
  67. Washburn JD, Cornell HV (1979) Chalcid parasitoid attack on a gall wasp population (Acraspis hirta (Hymenoptera: Cynipidae)) on Quercus prinus (Fagaceae). Can Ento 111:391–400Google Scholar
  68. Washburn JD, Cornell HV (1981) Parasitoids, patches, and phenology: their possible role in the local extinction of a cynipid gall wasp population. Ecology 62:1597–1607Google Scholar
  69. Weld LH (1957) Cynipid galls of the Pacific slope. Ann Arbor (Privately printed)Google Scholar
  70. Weld LH (1959) Cynipid galls of the eastern United States. Ann Arbor (Privately printed)Google Scholar
  71. Weld LH (1960) Cynipid galls of the southwest. Ann Arbor (Privately printed)Google Scholar
  72. Williams AH (1963) Enzyme inhibition by phenolic compounds. In: Enzyme chemistry of phenolic compounds. Pridham JB (ed) Pergamon Press, Oxford, and Macmillan, New YorkGoogle Scholar
  73. Wratten SD, Goddard P, Edwards PJ (1981) British trees and insects: the role of palatability. Am Nat 118:916–919Google Scholar
  74. Zar JH (1984) Biostatistical analysis, 2nd edition. Prentice-Hall, Englewood Cliffs, NJGoogle Scholar
  75. Zucker WV (1983) Tannins: Does structure determine function? An ecological perspective. Am Nat 121:335–365Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • M. L. Taper
    • 1
  • T. J. Case
    • 2
  1. 1.Institute of Biological SciencesTsukuba UniversityIbarakiJapan
  2. 2.Dept. of BiologyUniversity of California at San DiegoLa JollaUSA

Personalised recommendations