Oecologia

, Volume 96, Issue 4, pp 537–547

Phenotypic variation in seedlings of a “keystone” tree species (Quercus douglasii): the interactive effects of acorn source and competitive environment

  • K. J. Rice
  • D. R. Gordon
  • J. L. Hardison
  • J. M. Welker
Original Papers

Abstract

Blue oak (Quercus douglasii) is a deciduous tree species endemic to California that currently exhibits poor seedling survival to sapling age classes. We used common garden techniques to examine how genetic variation at regional and local scales affected phenotypic expression in traits affecting oak seedling growth and survival. Between-population variation was examined for seedlings grown from acorns collected from a northern, mesic population and a southern, xeric population. Within-population variation was examined by comparing seedlings from different maternal families within the mesic population. Acorns were planted into neighborhoods of an annual dicot (Erodium botrys), an annual grass (Bromus diandrus), and a perennial bunchgrass (Nassella pulchra). By varying the species composition of herbaceous neighborhoods into which acorns were planted, the interactive effects of competition and acorn germplasm source on phenotypic expression could also be examined. Potential maternal effects, expressed as variation in acorn size, were assessed by weighing each acorn before planting. Probability of seedling emergence increased significantly with acorn size in the xeric population but not in the mesic population. Similarly, the effect of acorn size on seedling leaf area, stem weight, and root weight was also population-dependent. At a within-population level, acorn size effects on seedling traits varied significantly among maternal families. In addition to acorn size effects, rates of oak seedling emergence were also dependent on an interaction of population source and competitive environment. Interactions between maternal family and competitive environment in the expression of seedling leaf characters suggest the possibility of genetic variation for plasticity in traits such as specific leaf area. Using carbon isotope discrimination (Δ) as an index of relative water-use efficiency (WUE), higher water use efficiency was indicated for oak seedlings grown in the annual plant neighborhoods compared to seedlings grown in the bunchgrass neighborhood. This trend may represent an adaptive plastic response because, compared to the bunchgrass neighborhood, soil water depletion was more rapid within annual plant neighborhoods.

Key words

Ecological genetics Phenotypic plasticity Plant competition Quercus douglasii Stable carbon isotope discrimination 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alexander HM, Wulff RD (1985) Experimental ecological genetics in Plantago. X The effects of maternal temperature on seed and seedling characters in P. lanceolata. J Ecol 73:271–282Google Scholar
  2. Antlfinger AE (1981) The genetic basis of microdifferentiation in natural and experimental populations of Borrichia frutescens in relation to salinity. Evolution 35:1056–1068Google Scholar
  3. Bolsinger CL (1988) The hardwoods of California timberlands, woodlands and savannahs. Res Bull PNW-RB-148USDA, Pac NW For Range Exp StaGoogle Scholar
  4. Bradshaw AD (1959) Population differentiation in Agrostis tenuis Sibth. I Morphological differentiation. New Phytol 58:208–227Google Scholar
  5. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155Google Scholar
  6. Bradshaw AD (1972) Some of the evolutionary consequences of being a plant. Evol Biol 5:25–47Google Scholar
  7. Bradshaw AD (1984) Ecological significance of genetic variation between populations. In: Dirzo R, Sarukhan J (eds) Perspectives on plant population ecology. Sinauer, MA, pp 213–228Google Scholar
  8. Brown RW, Bartos DL (1982) A calibration model for screen-caged Peltier thermocouple psychrometers. USDA For Serv Res Pap INT-293, Intermt For Range Exp Stn, Ogden, UTGoogle Scholar
  9. Callaway RM (1992a) Morphological and physiological responses of three California oak species to shade. Int J Plant Sci 153:434–441Google Scholar
  10. Callaway RM (1992b) Effects of shrubs on recruitment of Quercus douglasii and Quercus lobata in California. Ecology 73:2118–2128Google Scholar
  11. Clausen J, Keek DD, Hiesey WM (1940) Experimental studies on the nature of species. I The effect of varied environments on western American plants. Carnegie Inst Washington Publ 581Google Scholar
  12. Cody ML (1986) Diversity, rarity, and conservation in Mediterranean-climate regions. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, MA, pp 122–152Google Scholar
  13. Cohen D (1970) The expected efficiency of water utilization in plants under different competition and selection regimes. Israel J Bot 19:50–54Google Scholar
  14. Condon AG, Farquhar GD, Richards RA (1990) Genotypic variation in carbon isotope discrimination in transpiration efficiency in wheat. I Leaf gas exchange and whole plant studies. Aust J Plant Physiol 17:9–22Google Scholar
  15. Conover WJ, Ohmann RJ (1981) Rank transformations as a bridge between parametric and non-parametric statistics. Am Stat 35:124–133Google Scholar
  16. Cook RE (1979) Patterns of juvenile mortality and recruitment in plants. In: Solbrig OT, Jain SK, Johnson GB, Raven PH (eds) Topics in plant population biology. Columbia University Press, NY, pp 207–231Google Scholar
  17. Cook SA (1962) Genetic system, variation, and adaptation in Eschscholzia californica. Evolution 16:278–299Google Scholar
  18. Cornell HV (1986) Oak species attributes and host size influence cynipine wasp species richness. Ecology 67:1582–1592Google Scholar
  19. Donavan LA, Ehleringer JR (1991) Ecolphysiological differences among juvenile and reproductive plants of several woody species. Oecologia 86:594–597Google Scholar
  20. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology-field methods and instrumentation. Chapman and Hall, London, pp 281–300Google Scholar
  21. Ehleringer JR, Schulze E-D, Ziegler H, Lange OL, Farquhar GD, Cowan IR (1985) Xylem-tapping mistletoes: water or nutrient parasites? Science 227:1479–1481Google Scholar
  22. Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552Google Scholar
  23. Farquhar GD, O'Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137Google Scholar
  24. Farquhar GD, Hubick KT, Condon AG, Richards RA (1988) Carbon isotope fractionation and plant water0use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Ecological Studies Vol 68, Springer-Verlag, NY, pp 21–40Google Scholar
  25. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Physiol 40:503–537Google Scholar
  26. Fortmann L, Huntsinger L (1987) Managing California's oak woodlands: a sociological study of owners. In: Plumb TR, Pillsbury NH (eds) Proceedings of the Symposium on Multiple-Use Management of California's Hardwood Resources; Nov. 12–14, 1986. San Luis Obispo, California. Gen Tech Rep PSW-100, For Range Exp Stn, Forest Service, USDA. Berkeley, CA pp 379–384Google Scholar
  27. Freund RJ, Littell RC, Spector PC (1986) SAS system for linear models. SAS Institute Inc, Cary, NCGoogle Scholar
  28. Geber MA, Dawson TE (1990) Genetic variation in and covariation between leaf gas exchange, morphology, and development in Polygonum arenastrum, an annual plant. Oecologia 85:153–158Google Scholar
  29. Gordon DR, Rice KJ (1993) Competitive effects of grassland annuals on soil water and blue oak (Quercus douglasii) seedlings. Ecology 74:68–82Google Scholar
  30. Gordon DR, Welker JM, Menke JW, Rice KJ (1989) Competition for soil water between annual plants and blue oak (Quercus douglasii) seedlings. Oecologia 79:533–541Google Scholar
  31. Gordon DR, Rice KJ, Welker JM (1991) Soil water effects on blue oak seedling establishment. In: Standiford RB (ed) Proceedings of the Symposium on Oak Woodlands and Hardwood Rangeland Management; Oct. 31-Nov. 2, 1990, Davis, California. Gen Tech Rep PSW-126, Pac SW Res Stn, USDA, Berkeley, CA pp 54–58Google Scholar
  32. Grace JB (1985) Juvenile vs. adult competitive abilities in plants: size-dependence in cattails (Typha). Ecology 66: 1630–1638Google Scholar
  33. Hall AE, Mutters RG, Hubick KT, Farquhar GD (1990) Genotypic differences in carbon isotope discrimination by cowpea under wet and dry field conditions. Crop Sci 30:300–305Google Scholar
  34. Hamrick JJ, Blanton HM, Hamrick KJ (1989) Genetic structure of geographically marginal populations of ponderosa pine. Am J Bot 76:1559–1568Google Scholar
  35. Hartgerink AP, Bazzaz FA (1984) Seedling-scale environmental heterogeneity influences individual fitness and population structure. Ecology 65: 198–206Google Scholar
  36. Harper JL (1977) Population biology of qlants. Academic Press, London, 892 p Heady HF (1958) Vegetational changes in the California annual type. Ecology 39:402–416Google Scholar
  37. Heslop-Harrison J (1964) Forty years of genecology. Adv Ecol Res 2: 159–247Google Scholar
  38. Hubick KT, Farquhar GD, Shorter R (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Aust J Plant Physiol 13:803–816Google Scholar
  39. Hubick KT, Shorter R, Farquhar GD (1988) Heritability and genotype x environment interactions of carbon isotope discrimination and transpirational efficiency in peanut (Arachis hypogaea L.). Aust J Plant Physiol 15:799–813Google Scholar
  40. Jackson LE, Roy J (1986) Growth patterns of mediterranean annual and perennial grasses under simulated rainfall regimes of southern France and California. Oecologia Plant 7: 191–212Google Scholar
  41. Jain SK, Bradshaw AD (1966) Evolutionary divergence among adjacent plant populations. I The evidence and its theoretical analysis. Heredity 21:407–441Google Scholar
  42. Johnson DA, Asay KH, Tieszen LL, Ehleringer JR, Jefferson PG (1990) Carbon isotope discrimination: potential in screening cool-season grasses for water-limited environments. Crop Sci 30:338–343Google Scholar
  43. Leverenz JW, Lev DJ (1987) Effects of carbon dioxide-induced climate changes on the natural ranges of six major commercial tree species in the western United States. In: Shands WE, Hoffman JS (eds) The Greenhouse Effect, Climate Change, and U.S. Forests. The Conservation Foundation, Washington, D.C. 304 pGoogle Scholar
  44. Levin DA, Kerster HW (1974) Gene flow in seed plants. Evol Biol 7:139–220Google Scholar
  45. Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton, NJ, 120 pGoogle Scholar
  46. Levins R, MacArthur RH (1966) The maintenance of genetic polymorphism in a spatially heterogeneous environment: variations on a theme by Howard Levene. Am Nat 100:585–589Google Scholar
  47. Libby WJ, Stettler RF, Setz FW (1969) Forest genetics and forest tree breeding. Ann Rev Gen 3:469–494Google Scholar
  48. Linhart YB, Mitton JB, Sturgeon KB, Davis ML (1981) Genetic variation in space and time in a population of ponderosa pine. Heredity 46:407–426Google Scholar
  49. Loach K (1967) Shade tolerance in tree seedlings. I Leaf photosynthesis and respiration in plants raised under artificial shade. New Phytol 66:607–621Google Scholar
  50. Loach K (1970) Shade tolerance in tree seedlings. II Growth analysis of plants raised under artificial shade. New Phytol 69:273–286Google Scholar
  51. McClaren MP, Bartolome JW (1989) Fire-related recruitment in stagnant Quercus douglasii populations. Can J For Res 19:580–585Google Scholar
  52. Madsen JL, Blake GM (1977) Ecological genetics of ponderosa pine in the northern Rocky Mountains. Silvae Gen 26:1–8Google Scholar
  53. Masle J, Farquhar GD (1988) Effects of soil strength on the relation of water-use efficiency and growth to carbon isotope discrimination in wheat seedlings. Plant Physiol 86:32–38Google Scholar
  54. Mazer SJ, Schick CT (1991) Constancy of population parameters for life history and floral traits in Raphanus sativus L. I Norms of reaction and the nature of genotype by environmental interactions. Heredity 67:143–156Google Scholar
  55. Mitton JB, Linhart YB, Hamrick JL, Beckman J (1977) Observations on genetic structure and mating systems in ponderosa pine of the Colorado Front Range. Theor Appl Gen 51:5–13Google Scholar
  56. Muick PC (1991) Effects of shade on blue oak and coast live oak regeneration in California annual grasslands. In: Standiford RB (ed) Proceedings of the Symposium on Oak Woodlands and Hardwood Rangeland Management; Oct. 31-Nov. 2, 1990, Davis, California. Gen Tech Rep PSW-126, Pac SW Res Stn, USDA, Berkeley, CA, pp 21–24Google Scholar
  57. Muick PC, Bartolome JW (1987) Factors associated with oak regeneraton in California. In: Plumb TR, Pillsbury NH (eds) Proceedings of the Symposium on Multiple-Use Management of California's Hardwood Resources; Nov. 12–14, 1986, San Luis Obispo, California. Gen Tech Rep PSW-100, For Range Exp Stn, Forest Service, USDA. Berkeley, CA, pp 86–91Google Scholar
  58. Ohmann JL, Mayer KE (1987) Wildlife habitats of California's hardwood forests: Linking extensive inventory data with habitat models. In: Plumb TR, Pillsbury NH (eds) Proceedings of the Symposium on Multiple-Use Management of California's Hardwood Resources; Nov. 12–14, 1986, San Luis Obispo, California. Gen Tech Rep PSW-100, For Range Exp Stn, Forest Service, USDA. Berkeley, CA, pp 174–182Google Scholar
  59. Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. J Anim Ecol 49:667–685Google Scholar
  60. Parrish JAD, Bazzaz FA (1985) Ontogenetic niche shifts in old-field annuals. Ecology 66:1296–1302Google Scholar
  61. Pearey RW, Pfitsch WA (1991) Influence of sunflecks on the δ13C of Adenocaulon bicolor plants occurring in contrsting forest understory microsites. Oecologia 86:457–462Google Scholar
  62. Read RA (1980) Genetic variation in seedling progeny of ponderosa pine provenances. For Sci Monogr 23:1–59Google Scholar
  63. Rehfeldt GE (1993) Genetic variation in the Ponderosae of the Southwest. Am J Bot 80(3):330–343Google Scholar
  64. Rice KJ, Mack RN (1991) Ecological genetics of Bromus tectorum. II Intraspecific variation in phenotypic plasticity. Oecologia 88:84–90Google Scholar
  65. Roach DA, Wulff RD (1987) Maternal effects in plants. Ann Rev Ecol Syst 18:209–235Google Scholar
  66. Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Ann Rev Ecol Syst. 17:667–693Google Scholar
  67. Schuster WSF, Phillips SL, Sandquist DR, Ehleringer JR (1992) Heritability of carbon isotope discrimination in Gutierrezia microcephala (Asteraceae). Am J Bot 79(2):216–221Google Scholar
  68. Smedley MP, Dawson TE, Comstock JP, Donovan LA, Sherril DE, Cook CS, Ehleringer JR (1991) Seasonal carbon isotope diserimination in a grassland community. Oecologia 85:314–320Google Scholar
  69. Solbrig OT (1981) Studies on the population biology of the genus Viola. II The effect of plant size on fitness in Viola sororia. Evolution 35:1080–1093Google Scholar
  70. Standiford RB, Diamond N, Passof PC, LeBlanc J (1987) Value of oaks in rural subdivisions. In: Plumb TR, Pillsbury NH (eds) Proceedings of the Symposium on Multiple-Use Management of California's Hardwood Resources; Nov. 12–14, 1986, San Luis Obispo, California. Gen Tech Rep PSW-100, For Range Exp Stn, Forest Service, USDA. Berkeley, CA, pp 156–160Google Scholar
  71. Stearns SC (1989) The evolutionary significance of phenotypic plasticity. BioScience 39:436–445Google Scholar
  72. Sternberg LSL, Mulkey SS, Wright SJ (1989) Ecological interpretation of leaf carbon isotope ratios: influence of respired carbon dioxide. Ecology 70(5):1317–1324Google Scholar
  73. Strauss-Debenedetti S, Bazzaz FA (1991) Plasticity and acclimation to light in tropical Moraceae of different successional positions. Oecologia 87:377–387Google Scholar
  74. Sultan SE (1987) Evolutionary implications of phenotypic plasticity in plants. Evol Biol 21:127–178Google Scholar
  75. Tecklin J, McCreary DD (1991) Acorn size as a factor in early seedling growth of blue oaks. In: Plumb TR, Pillsbury NH (eds) Proceedings of the Symposium on Multiple-Use Management of California's Hardwood Resources; Nov. 12–14, 1986, San Luis Obispo, California. Gen Tech Rep PSW-100, For Range Exp Stn, Forest Service, USDA. Berkeley, CA, pp 48–53Google Scholar
  76. Toft NL, Anderson JE, Nowak RS (1989) Water use efficiency and carbon isotope composition of plants in a cold desert environment. Oecologia 80:11–18Google Scholar
  77. Turresson G (1922) The genotypical response of the plant species to the habitat. Hereditas 3:211–350Google Scholar
  78. Verner J (1987) The importance of hardwood habitats for wildlife in California. In: Plumb TR, Pillsbury NH (eds) Proceedings of the Symposium on Multiple-Use Management of California's Hardwood Resources; Nov. 12–14, 1986, San Luis Obispo, California. Gen Tech Rep PSW-100, For Range Exp Stn, Forest Service, USDA. Berkeley, CA, pp 162–163Google Scholar
  79. Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522Google Scholar
  80. Welker JM, Gordon DR, Rice KJ (1991) Capture and allocation of nitrogen by Quercus douglasii seedlings in competition with annual and perennial grasses. Oecologia 87:459–466Google Scholar
  81. White KL (1966) Structure and composition of foothill woodland and central coastal California. Ecology 47:229–237Google Scholar
  82. Williams K, Richards JH, Caldwell MM (1991) Effect of competition on stable carbon isotope ratios of two tussock grass species. Oecologia 88:148–151Google Scholar
  83. Zangerl AR, Bazzaz FA (1983) Responses of an early and a late successional species of Polygonum to variation in resource availability. Oecologia 56:397–404Google Scholar
  84. Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, NJ, 718 pGoogle Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • K. J. Rice
    • 1
  • D. R. Gordon
    • 1
  • J. L. Hardison
    • 1
  • J. M. Welker
    • 1
  1. 1.Department of Agronomy and Range ScienceUniversity of CaliforniaDavisUSA
  2. 2.The Nature Conservancy, Florida Museum of Natural HistoryUniversity of FloridaGainesvilleUSA
  3. 3.Natural Resources Ecology LabColorado State UniversityFt. CollinsUSA

Personalised recommendations