Plant Ecology

, Volume 217, Issue 7, pp 825–841 | Cite as

The impacts of isolation, canopy size, and environmental conditions on patterns of understory species richness in an oak savanna

  • Karen A. StahlheberEmail author


Fragmentation and habitat loss have transformative effects on landscapes. Like many savanna communities worldwide, California oak savannas (Quercus spp.) have experienced extensive anthropogenic clearing, increasing the isolation of individual trees. Isolation and tree size may have consequences for populations of understory plants, but this has never been evaluated in a temperate savanna community. I address two questions: (1) How does the presence of oak trees affect site-level species richness? (2) What landscape and/or local attributes are associated with trees that contribute many species to a site? Vegetation and environmental attributes in the understory of isolated oaks and in surrounding grassland were surveyed at four sites in California, USA. I counted the number of species occurring in plots underneath and at the edge of each tree that were absent from surrounding plots in open grassland (‘oak-associated species’). I used species-area curves to evaluate the contribution of oaks to site-level species richness. The importance of crown area, isolation, environmental heterogeneity, and understory soil fertility on species occurrences was assessed using linear mixed models. At two of the four sites, oaks increased site species richness by 23–57 %. At the southernmost site, understory soil fertility and isolation were negatively related to oak-associated species. Across all four sites, trees with larger crown area had more oak-associated species. Savanna oaks are important structuring forces for landscape plant species richness, especially in dry locations. Large trees may be especially important for conserving diverse understories. These positive effects, however, are not always negatively influenced by isolation.


Quercus Connectivity Crown area Species-area curve Environmental heterogeneity Island biogeography theory California Stress-gradient hypothesis 



This work was funded by a University of California Natural Reserve System Mildred E. Mathias Graduate Student Research Grant, a California Native Plant Society Educational Grant, and a National Science Foundation Dissertation Improvement Grant (DEB-1110569). The directors of the UC Reserves provided much needed logistical support and site knowledge: K. McCurdy, M. Stromberg, M. Hamilton, P. Aigner, and C. Koehler. Comments from C.M. D’Antonio, B. Mahall, J.M. Levine, and two anonymous reviewers on earlier versions of this manuscript were helpful, as well as suggestions from E. Damschen on data analysis.


  1. Accatino F, Wiegand K, Ward D, De Michele C (2016) Trees, grass, and fire in humid savannas: the importance of life history traits and spatial processes. Ecol Model 320:135–144CrossRefGoogle Scholar
  2. Allen-Diaz BH, Bartolome J, McClaran MP (1999) California oak savanna. In: Fralish JS, Baskin JM (eds) Savannas, barrens, and rock outcrop plant communities of North America. Cambridge University Press, Cambridge, pp 322–339CrossRefGoogle Scholar
  3. Báldi A (2008) Habitat heterogeneity overrides the species–area relationship. J Biogeogr 35:675–681CrossRefGoogle Scholar
  4. Baldwin BG, Goldman DH, Keil DJ, Patterson R, Rosatti TJ, Wilken DH (eds) (2012) The Jepson manual: vascular plants of California, 2nd edn. University of California Press, BerkeleyGoogle Scholar
  5. Bartolome JW, Allen-Diaz BH, Tietje WD (1994) The effect of Quercus douglasii removal on understory yield and composition. J Range Manage 47:151–154CrossRefGoogle Scholar
  6. Barton K (2015) MuMIn: Multi-model inference. R package version 1.13.4. March 2015
  7. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-6. March 2015
  8. Belsky AJ, Mwonga SM, Amundson RG, Duxbury JM, Ali AR (1993) Comparative effects of isolated trees on their undercanopy environments in high- and low-rainfall savannas. J Appl Ecol 30:143–155CrossRefGoogle Scholar
  9. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193CrossRefPubMedGoogle Scholar
  10. Bolsinger CL (1988) The hardwoods of California’s timberlands, woodlands, and savannas. USDA Forest Service. Pacific Northwest Region, Resource Bulletin PNW-RB-148. Portland, OregonGoogle Scholar
  11. Brose U (2001) Relative importance of isolation, area and habitat heterogeneity for vascular plant species richness of temporary wetlands in east-German farmland. Ecography 24:722–730CrossRefGoogle Scholar
  12. Burke MJW, Grime JP (1996) An experimental study of plant community invasibility. Ecology 77:776–790CrossRefGoogle Scholar
  13. Colwell RK, Chao A, Gotelli NJ, Lin SY, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5:3–21CrossRefGoogle Scholar
  14. Connor EF, McCoy ED (1979) The statistics and biology of the species-area relationship. Am Nat 113:791–833CrossRefGoogle Scholar
  15. Cousins SA (2006) Plant species richness in midfield islets and road verges–the effect of landscape fragmentation. Biol Conserv 127:500–509CrossRefGoogle Scholar
  16. Cousins SA, Ohlson H, Eriksson O (2007) Effects of historical and present fragmentation on plant species diversity in semi-natural grasslands in Swedish rural landscapes. Landscape Ecol 22:723–730CrossRefGoogle Scholar
  17. Dahlgren RA, Singer MJ, Huang X (1997) Oak tree and grazing impacts on soil properties and nutrients in a California oak woodland. Biogeochemistry 39:45–64CrossRefGoogle Scholar
  18. Davis MA, Pelsor M (2001) Experimental support for a resource-based mechanistic model of invasibility. Ecol Lett 4:421–428CrossRefGoogle Scholar
  19. de Lima Dantas V, Batalha MA, França H, Pausas JG (2015) Resource availability shapes fire-filtered savannas. J Veg Sci 26:395–403CrossRefGoogle Scholar
  20. Dean WRJ, Milton SJ, Jeltsch F (1999) Large trees, fertile islands, and birds in arid savanna. J Arid Environ 41:61–78CrossRefGoogle Scholar
  21. Dohn J, Dembélé F, Karembé M, Moustakas A, Amévor KA, Hanan NP (2013) Tree effects on grass growth in savannas: competition, facilitation and the stress-gradient hypothesis. J Ecol 101:202–209CrossRefGoogle Scholar
  22. Eriksson O (1996) Regional dynamics of plants: a review of evidence for remnant, source-sink and metapopulations. Oikos 77:248–258CrossRefGoogle Scholar
  23. Facelli JM, Brock DJ (2000) Patch dynamics in arid lands: localized effects of Acacia papyrocarpa on soils and vegetation of open woodlands of south Australia. Ecography 23:479–491CrossRefGoogle Scholar
  24. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  25. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Global Ecol Biogeogr 16:265–280CrossRefGoogle Scholar
  26. Freckleton RP, Watkinson AR (2002) Large-scale spatial dynamics of plants: metapopulations, regional ensembles and patchy populations. J Ecol 90:419–434CrossRefGoogle Scholar
  27. Gallardo A (2003) Effect of tree canopy on the spatial distribution of soil nutrients in a Mediterranean dehesa. Pedobiologia 47:117–125CrossRefGoogle Scholar
  28. Graae BJ, Sunde PB (2000) The impact of forest continuity and management on forest floor vegetation evaluated by species traits. Ecography 23:720–731CrossRefGoogle Scholar
  29. Hanski I (1998) Metapopulation dynamics. Nature 396:41–49CrossRefGoogle Scholar
  30. Harner RF, Harper KT (1976) The role of area, heterogeneity, and favorability in plant species diversity of pinyon-juniper ecosystems. Ecology 57:1254–1263CrossRefGoogle Scholar
  31. Harrison S (1999) Native and alien species diversity at the local and regional scales in a grazed California grassland. Oecologia 121:99–106CrossRefGoogle Scholar
  32. Higgins SI, Pickett STA, Bond WJ (2000) Predicting extinction risks for plants: environmental stochasticity can save declining populations. Trends Ecol Evol 15:516–520CrossRefPubMedGoogle Scholar
  33. Higgins SI, Lavorel S, Revilla E (2003) Estimating plant migration rates under habitat loss and fragmentation. Oikos 101:354–366CrossRefGoogle Scholar
  34. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337CrossRefGoogle Scholar
  35. Hobbs RJ, Yates CJ (2003) Turner Review No. 7. Impacts of ecosystem fragmentation on plant populations: generalising the idiosyncratic. Aust J Bot 51:471–488CrossRefGoogle Scholar
  36. Holl KD, Crone EE (2004) Applicability of landscape and island biogeography theory to restoration of riparian understorey plants. J Appl Ecol 41:922–933CrossRefGoogle Scholar
  37. Holmgren M, Scheffer M (2010) Strong facilitation in mild environments: the stress gradient hypothesis revisited. J Ecol 98:1269–1275CrossRefGoogle Scholar
  38. Honnay O, Hermy M, Coppin P (1999) Effects of area, age and diversity of forest patches in Belgium on plant species richness, and implications for conservation and reforestation. Biol Conserv 87:73–84CrossRefGoogle Scholar
  39. Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491CrossRefGoogle Scholar
  40. Joshi J, Stoll P, Rusterholz HP, Schmid B, Dolt C, Baur B (2006) Small-scale experimental habitat fragmentation reduces colonization rates in species-rich grasslands. Oecologia 148:144–152CrossRefPubMedGoogle Scholar
  41. Kirkman LK, Mitchell RJ, Helton RC, Drew MB (2001) Productivity and species richness across an environmental gradient in a fire-dependent ecosystem. Am J Bot 88:2119–2128CrossRefPubMedGoogle Scholar
  42. Kiviniemi K, Eriksson O (1999) Dispersal, recruitment and site occupancy of grassland plants in fragmented habitats. Oikos 86:241–253CrossRefGoogle Scholar
  43. Ko LJ, Reich PB (1993) Oak tree effects on soil and herbaceous vegetation in savannas and pastures in Wisconsin. Am Midl Nat 130:31–42CrossRefGoogle Scholar
  44. Kolb A, Diekmann M (2005) Effects of life-history traits on responses of plant species to forest fragmentation. Conserv Biol 19:929–938CrossRefGoogle Scholar
  45. Krauss J, Klein AM, Steffan-Dewenter I, Tscharntke T (2004) Effects of habitat area, isolation, and landscape diversity on plant species richness of calcareous grasslands. Biodivers Conserv 13:1427–1439CrossRefGoogle Scholar
  46. Kuznetsova A, Brockhoff PB, Christensen RHB (2014). lmerTest: Tests in Linear Mixed Effects Models. R package version 2.0-20. March 2015
  47. Legendre P, Legendre LF (2012) Numerical ecology, 3rd edn. Elsevier, AmsterdamGoogle Scholar
  48. Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecology 85:1840–1845CrossRefGoogle Scholar
  49. Lindsdale JM (1943) Human relations to the Hastings Reservation in the past [with information on land use and its influence on vegetation]. Hastings Natural History Reservation. Accessed 10 April 13
  50. López RP, Larrea-Alcázar DM, Teresa O (2009) Positive effects of shrubs on herbaceous species richness across several spatial scales: evidence from the semiarid Andean subtropics. J Veg Sci 20:728–734CrossRefGoogle Scholar
  51. Ludwig F, de Kroon H, Berendse F, Prins HHT (2004) The influence of savanna trees on nutrient, water and light availability and the understorey vegetation. Plant Ecol 170:93–105CrossRefGoogle Scholar
  52. MacArthur R, Wilson EO (1967) The theory of island biogeography. Princeton University Press, PrincetonGoogle Scholar
  53. Maestre FT, Cortina J (2005) Remnant shrubs in Mediterranean semi-arid steppes: effects of shrub size, abiotic factors and species identity on understorey richness and occurrence. Acta Oecol 27:161–169CrossRefGoogle Scholar
  54. Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205CrossRefGoogle Scholar
  55. Mahall BE, Tyler CM, Cole ES, Mata C (2009) A comparative study of oak (Quercus, Fagaceae) seedling physiology during summer drought in southern California. Am J Bot 96:751–761CrossRefPubMedGoogle Scholar
  56. Malo J, Suárez F (1995) Herbivorous mammals as seed dispersers in a Mediterranean dehesa. Oecologia 104:246–255CrossRefGoogle Scholar
  57. Manning AD, Fischer J, Lindenmayer DB (2006) Scattered trees are keystone structures—implications for conservation. Biol Conserv 132:311–321CrossRefGoogle Scholar
  58. Maron JL, Connors PG (1996) A native nitrogen-fixing shrub facilitates weed invasion. Oecologia 105:302–312CrossRefGoogle Scholar
  59. Matthews JW, Peralta AL, Flanagan DN, Baldwin PM, Soni A, Kent AD, Endress AG (2009) Relative influence of landscape vs. local factors on plant community assembly in restored wetlands. Ecol Appl 19:2108–2123CrossRefPubMedGoogle Scholar
  60. McClaran MP, Bartolome JW (1989) Effect of Quercus douglasii (Fagaceae) on herbaceous understory along a rainfall gradient. Madroño 36:141–153Google Scholar
  61. McCune J, Vellend M (2015) Using plant traits to predict the sensitivity of colonizations and extirpations to landscape context. Oecologia 178:511–524CrossRefPubMedGoogle Scholar
  62. Mclaughlin Natural Reserve (2009) Land use—nineteenth century history. Accessed 10 April 13
  63. McLaughlin BC, Zavaleta ES (2013a) Regional and temporal patterns of natural recruitment in a California endemic oak and a possible ‘research reserve effect’. Divers Distrib 19:1440–1449CrossRefGoogle Scholar
  64. McLaughlin BC, Zavaleta ES (2013b) Shifting bottom-up and top-down regulation of oak recruitment across a regional resource gradient. Global Ecol Biogeogr 22:718–727CrossRefGoogle Scholar
  65. McNaughton SJ (1968) Structure and function in California grasslands. Ecology 49:962–972CrossRefGoogle Scholar
  66. Moustakas A, Sakkos K, Wiegand K, Ward D, Meyer KM, Eisinger D (2009) Are savannas patch-dynamic systems? A landscape model. Ecol Model 220:3576–3588CrossRefGoogle Scholar
  67. Murphy HT, Lovett-Doust J (2004) Context and connectivity in plant metapopulations and landscape mosaics: does the matrix matter? Oikos 105:3–14CrossRefGoogle Scholar
  68. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  69. Natural Resources Conservation Service (2013) United States Department of Agriculture. Web Soil Survey. Accessed 16 July 2013
  70. Öster M, Cousins SA, Eriksson O (2007) Size and heterogeneity rather than landscape context determine plant species richness in semi-natural grasslands. J Veg Sci 18:859–868CrossRefGoogle Scholar
  71. Ovalle C (1987) Interactions of the tree layer with the herbaceous layer in Chile. Part I: effect of trees on the floristic composition, productivity and phenology of the herbaceous layer. Acta Oecol Oecol Plant 8:385–404Google Scholar
  72. Parker VT, Muller CH (1982) Vegetational and environmental changes beneath isolated live oak trees (Quercus agrifolia) in a California annual grassland. Am Midl Nat 107:69–81CrossRefGoogle Scholar
  73. Petit S, Griffiths L, Smart SS, Smith GM, Stuart RC, Wright SM (2004) Effects of area and isolation of woodland patches on herbaceous plant species richness across Great Britain. Landscape Ecol 19:463–471CrossRefGoogle Scholar
  74. Quinn JF, Robinson GR (1987) The effects of experimental subdivision on flowering plant diversity in a California annual grassland. J Ecol 75:837–855CrossRefGoogle Scholar
  75. Ribeiro PJ, Diggle PJ (2001) geoR: a package for geostatistical analysis. R-NEWS, 1(2):15–18. March 2015
  76. Riginos C, James BG, David JA, Truman PY (2009) Local versus landscape-scale effects of savanna trees on grasses. J Ecol 97:1337–1345CrossRefGoogle Scholar
  77. Roche LM, Rice KJ, Tate KW (2012) Oak conservation maintains native grass stands in an oak woodland-annual grassland system. Biodivers Conserv 21:2555–2568CrossRefGoogle Scholar
  78. Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32CrossRefGoogle Scholar
  79. Schleicher J, Meyer KM, Wiegand K, Schurr FM, Ward D (2011) Disentangling facilitation and seed dispersal from environmental heterogeneity as mechanisms generating associations between savanna plants: Cause of spatial associations of savanna plant species. J Veg Sci 22:1038–1048CrossRefGoogle Scholar
  80. Scholes RJ, Archer SR (1997) Tree-grass interactions in savannas. Annu Rev Ecol Syst 28:517–544CrossRefGoogle Scholar
  81. Seabloom EW, Borer ET, Martin BA, Orrock JL (2009) Effects of long-term consumer manipulations on invasion in oak savanna communities. Ecology 90:1356–1365CrossRefPubMedGoogle Scholar
  82. Shipman GE (1972) Soil survey of northern Santa Barbara area, California. United States Department of Agriculture, Soil Conservation Service, California Agricultural Experiment StationGoogle Scholar
  83. Sork VL, Davis FW, Smouse PE, Apsit VJ, Dyer RJ, Fernandez-M JF, Kuhn B (2002) Pollen movement in declining populations of California Valley oak, Quercus lobata: where have all the fathers gone? Mol Ecol 11:1657–1668CrossRefPubMedGoogle Scholar
  84. Stahlheber, K.A. (2013). The influence of savanna oaks on California grassland plant composition. Dissertation, University of California, Santa BarbaraGoogle Scholar
  85. Stahlheber KA, Crispin KL, Anton C, D’Antonio CM (2015) The ghosts of trees past: savanna trees create enduring legacies in plant species composition. Ecology 96:2510–2522CrossRefPubMedGoogle Scholar
  86. Tyler CM, Kuhn B, Davis FW (2006) Demography and recruitment limitations of three oak species in California. Q Rev Biol 81:127–152CrossRefPubMedGoogle Scholar
  87. Tyler CM, Davis FW, Mahall BE (2008) The relative importance of factors affecting age-specific seedling survival of two co-occurring oak species in southern California. For Ecol Manag 255:3063–3074CrossRefGoogle Scholar
  88. Vellend M, Verheyen K, Flinn KM, Jacquemyn H, Kolb A, Van Calster H, Peterken G, Graae BJ, Bellemare J, Honnay O, Brunet J, Wulf M, Gerhardt F, Hermy M (2007) Homogenization of forest plant communities and weakening of species–environment relationships via agricultural land use. J Ecol 95:565–573CrossRefGoogle Scholar
  89. Verheyen K, Honnay O, Motzkin G, Hermy M, Foster DR (2003) Response of forest plant species to land-use change: a life-history trait-based approach. J Ecol 91:563–577CrossRefGoogle Scholar
  90. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  91. Ward D, Wiegand K, Getzin S (2013) Walter’s two-layer hypothesis revisited: back to the roots! Oecologia 172:617–630CrossRefPubMedGoogle Scholar
  92. Whipple AA, Grossinger RM, Davis FW (2010) Shifting baselines in a California oak savanna: nineteenth century data to inform restoration scenarios. Rest Ecol 19:81–101Google Scholar
  93. Wiegand K, Saltz D, Ward D (2006) A patch-dynamics approach to savanna dynamics and woody plant encroachment—Insights from an arid savanna. Perspect Plant Ecol Evol Syst 7:229–242CrossRefGoogle Scholar
  94. Wilcox JT (2000) A history of Blue Oak Ranch Reserve. In Hamilton M (ed) Accessed 10-4-13
  95. Williamson M (1989) Guest Editorial: The MacArthur and Wilson theory today: true but trivial. J Biogeogr 16:3–4Google Scholar
  96. Zavaleta ES, Hulvey KB, Fulfrost B (2007) Regional patterns of recruitment success and failure in two endemic California oaks. Divers Distrib 13:735–745CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Ecology, Evolution and Marine BiologyUniversity of California Santa BarbaraSanta BarbaraUSA
  2. 2.W. K. Kellogg Biological StationMichigan State UniversityHickory CornersUSA

Personalised recommendations