Trees (1997) 11: 169–175 Springer-Verlag 1997 ORIGINAL ARTICLE John C. Hunter gorrespondene of environmentl tolernes with lef nd rnh ttriutes for six oEourring speies of rodlef evergreen trees in northern gliforni Accepted: 22 March 1996 AbstractmFor the angiosperm dominants of northern Cali- fornia’s mixed evergreen forests, this study compares the sntrodution display of photosynthetic tissue within leaves and along branches, and examines the correspondence between these The display of photosynthetic tissue at the levels of leaf, morphological attributes and the known environmental branch and entire crown strongly influences the ecophys- tolerances of these species. Measurements were made on iology of trees (Kozlowski et al. 1991). Leaf size and both sun and shade saplings of six species: Arbutus men- structure influence virtually all above-ground plant-envi- ziesii (Ericaceae), Chrysolepis chrysophylla (Fagaceae), ronment interactions including energy balance, gas ex- Lithocarpus densiflorus (Fagaceae), Quercus chrysolepis change and herbivory, and determine the cost of packaging (Fagaceae), Quercus wislizenii (Fagaceae), and photosynthetic tissue into leaves (Givnish 1979; Nobel Umbellularia californica (Lauraceae). All species had 1983; Metcalfe 1983). Together with leaf form and anat- sclerophyllous leaves with thick epidermal walls, but spe- omy, branch architecture determines the distribution of cies differed in leaf specific weight, thickness of mesophyll photosynthetic tissue in space and the cost of displaying tissues and in the presence of a hypodermis, crystals, that tissue along stems (White 1983; Ku¨ppers 1985, 1989; secretory idioblasts, epicuticular deposits, and trichomes. Canham 1988). Furthermore, because of the semi-autono- The leaves of Arbutus were 2–5 times larger than those of mous nature of branches (Sprugel et al. 1991), the entire Chrysolepis, Lithocarpus and Umbellularia and 4–10 times crown’s attributes are, to a degree, the summation of the larger than those of both Quercus species. Together with attributes of the branches and of the leaves they bear differences in branch architecture, these leaf traits divide (Zimmerman and Brown 1971; Halle et al. 1978) the species into groups corresponding to environmental The purpose of this study is to compare the display of tolerances. Shade-tolerant Chrysolepis, Lithocarpus, and photosynthetic tissue within leaves and along branches of Umbellularia had longer leaf lifespans and less palisade six co-occurring tree species, and to examine the corre- tissue, leaf area, and crown mass per volume than the spondence between known differences in environmental intermediate to intolerant Arbutus and Quercus. Having tolerances and measured differences in leaf structure and smaller leaves, Quercus branches had more branch mass branch architecture. The six species are: Arbutus menziesii per leaf area and per palisade volume than other species, (madrone, Ericaceae), Chrysolepis chrysophylla (giant whereas Arbutus had less than other species. These differ- chinquapin, Fagaceae), Lithocarpus densiflorus (tan oak, ences in display of photosynthetic tissue should contribute Fagaceae), Quercus chrysolepis (canyon live oak, Faga- to greater growth for Quercus relative to the other species ceae), Q. wislizenii (interior live oak, Fagaceae), and under high light and limited water, for Arbutus under high Umbellularia californica (California bay, Lauraceae). light and water availability, and for Chrysolepis, Lithocar- They constitute the evergreen angiosperm component of pus, and Umbellularia under limiting light levels. California’s mixed evergreen forests, which are co-domi- nated by conifers and are the predominant forest vegetation where elevation or coastal fog does not ameliorate Cali- c Key wordsmBranch architecture c Leaf anatomy Leaf fornia’s Mediterranean climate (Barbour and Major 1977). c longevity c Leaf specific weight Tree morphology There are known differences in environmental toler- ances among these species. The Quercus species are dis- J. C. Hunter1 tributed into more xeric habitats than the other species Plant Biology Section, University of California, Davis, USA (Jepson 1899, 1910; Griffin and Critchfield 1972; Myatt Present address: 1975), and within mixed evergreen forests the Quercus 1 Department of Biological Sciences, State University of New York, species are most abundant on more xeric sites (Waring College at Brockport, Brockport, NY 14420, USA 170 and Major 1964; Whittaker 1960; Sawyer et al. 1977; Leaf structure measurements Campbell 1980). Arbutus and both Quercus species are For each species, 33 leaves were randomly selected from the upper considered to be of low to intermediate shade-tolerance, third of the crown of each of six saplings (n = 198 leaves). Three of the whereas Chrysolepis, Lithocarpus and Umbellularia are saplings grew in full sun and three beneath the closed canopy of the considered shade-tolerant (Jepson 1910; Unsicker 1974; forest. Dale and Hemstrom 1984; Tappeiner et al. 1990; Keeler- The area of 30 of the leaves from each sapling was determined using a Li-Cor LI-3100 automatic planimeter. These leaves subse- Wolf 1988; McKee 1990; Stein 1990; Thornburgh 1990). quently were dried at 100 °C for 1 h and then at 70 °C until weight loss These interpretations of shade-tolerance are supported by ceased. The mass of each leaf was determined using a Mettler AE100 the relative abundance of saplings in high and low light balance. From these measures, the average leaf area and specific microsites (Waring and Major 1964; Hunter 1995) and by weight (g/cm2) were calculated. rates of sapling survival and growth in forest understories From the remaining three leaves of each sapling, free hand sections were taken from the middle of the blade half way between mid-rib and (Pelton 1962; Tappeiner et al. 1986; Hunter 1995; J.C. margin. The sections were lightly stained with toluidine blue and Hunter, unpublished work). examined at 400×. A general description of leaf structure was However, little is known about the display of photosyn- recorded, and on a representative segment of each leaf section, total thetic tissues by these species. For all six species, leaf shape mesophyll thickness, palisade thickness, and thickness of the outer and the range of leaf length and width are documented epidermal wall were measured using a calibrated reticel for scale. (Hickman 1993). For some species, there also are descrip- tions of leaf anatomy (Cooper 1922; Kasapligil 1951) or Branch architecture measurements observations on leaf longevity (Sudworth 1908). Quantita- tive measures of leaf area generally are lacking and there For each species, six branches were randomly selected from the are no descriptions of branch architecture. periphery of the upper third of the crown of each of six saplings (n = 36 branches). Three of the saplings grew in full sun and three This existing information is insufficient to make an beneath the closed canopy of the forest. interspecific comparison of the display of photosynthetic After the growing season, 1 year’s growth was removed from each tissue. Therefore, this study was designed to fill that gap branch (from most recent bud scar to shoot tip). Elongation (the stem with information on leaf form and branch architecture of segment’s length) was measured, as was each leaf’s length from petiole base to blade tip. Leaf blades were removed and their area measured each species in both sun and shade. I use these measure- with a Li-Cor LI-3100 automatic planimeter. Afterwards, both leaf ments to compare the display of photosynthetic tissue by blades and branch segments with petioles were dried at 100 °C for 1 h these species, and to examine the relationships between and then at 70 °C until weight loss ceased. For each branch, mass of these leaf and branch attributes and the known environ- leaf blades and of the stem segment with petioles was determined with a Mettler AE100 balance. mental tolerances of the species. From these measures, volume occupied, leaf area per unit volume, and total crown mass (leaves plus stem) per unit volume were calculated. For these calculations, volume occupied by a branch was treated as a cylinder and considered to equal: 3.14 (branch length) (average leaf length)2. Because most chloroplasts are within palisade tissue (Fahn 1982), wterils nd methods palisade volume per volume occupied by a branch also was used as a measure of photosynthetic tissue distribution (in addition to leaf area Study site and mass). Palisade volume per unit volume was calculated as: (average palisade thickness)(leaf area of branch)/(volume occupied All measurements were made on plants growing between 430 and by branch). 550 m on Hugo soils (Inceptisols) at the University of California’s On an additional ten branches per plant selected randomly, branch Northern California Coast Range Preserve in Mendocino County (39° extension growth and number of leaf cohorts per branch were recorded. ° W 35W N 123 37 W). Most of the preserve is covered with mixed- Leaf longevity also was estimated using petiole scars and bud scars to evergreen forest dominated by the conifer Pseudotsuga menziesii and determine leaf retention per cohort for a random sample of 25 branches the broadleaf evergreen trees of this study. from throughout the crown of 15 fallen canopy trees (three of each On the preserve, the local distribution of the broadleaf evergreen species except Q. chrysolepis of which no fallen trees were available). trees is representative