Trees (1997) 11: 169–175  Springer-Verlag 1997

ORIGINAL ARTICLE

John C. Hunter

gorresponden™e of environment—l toler—n™es with le—f —nd ˜r—n™h

—ttri˜utes for six ™oEo™™urring spe™ies of ˜ro—dle—f evergreen trees in northern g—liforni—

Accepted: 22 March 1996

AbstractmFor the angiosperm dominants of northern Cali- fornia’s mixed evergreen forests, this study compares the sntrodu™tion 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), w—teri—ls —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 of California’s northern coastal region (Waring and Major 1964; Sawyer et al. 1977; Wainwright and Barbour 1984). Lithocarpus densiflorus and Arbutus menziesii dominate on north-

facing slopes. On south-facing slopes, Lithocarpus is far less abundant and Quercus chrysolepis and Q. wislizenii are dominants along with ‚esults Arbutus.(Chrysolepis and Umbellularia are both widely distributed but only locally abundant.) Leaf structure In the understory, growth, abundance and distribution of these trees reflect their shade-tolerance as reported in other studies (Jepson 1910; Unsicker 1974; Dale and Hemstrom 1984; Keeler-Wolf 1988; Tappei- Despite some commonalities, species differed substantially ner et al. 1990; McKee 1990; Stein 1990; Thornburgh 1990). Saplings in the packaging of photosynthetic tissue within leaves. of Arbutus are rarely present. Saplings of Q. wislizenii are often Leaf area, thickness of mesophyll tissues, and the relation present, but rarely reach a meter in height. Saplings of Q. chrysolepis

are more widespread and abundant, and occasionally reach larger size of mesophyll thickness to specific weight differed among classes (R 1 m). However, only Chrysolepis, Lithocarpus and Umbel- species. All species had sclerophyllous leaves and an lularia regularly survive into larger size classes in the understory. epidermis with thick outer walls, and none had stomatal crypts, sunken stomata or amphistomatic leaves. Minor and major veins were sheathed with fibers and fiber-tracheids, and extensions of the sheaths extended to both epidermises. 171

Among sun leaves (Table 1), Arbutus had a significantly

thicker mesophyll (271C55 µm) than all but Q. wislizenii

(239C64 µm; other species 189–215 µm), and had a thicker palisade tissue (151C47 µm) than all other species (76–122 µm). Sun leaves of Q. wislizenii and Chrysolepis had a significantly thicker palisade tissue than Q. chryso- lepis, which in turn was significantly thicker than Litho- carpus and Umbellularia (Tukey test P = 0.05). Sun leaves of Lithocarpus and Umbellularia had significantly thinner mesophylls and palisade tissues than those of other species Fig. 1mSun and shade leaf area of broadleaf evergreen tree species at (Tukey test, P = 0.05). the Northern California Coast Range Preserve, Mendocino County. Among shade leaves, there were fewer interspecific [AM = Arbutus menziesii, CC = Chrysolepis chrysophylla, LD = differences in mesophyll thickness than among sun leaves Lithocarpus densiflorus, QC = Quercus chrysolepis, QW = Quercus (Table 1). Arbutus had a significantly thicker mesophyll

wislizenii, UC = Umbellularia californica. Error bar represents 1 SE (202C19 µm) than other species (127–149 µm), and that (n = 90)]

thicker mesophyll had a thicker palisade tissue as well (74C14 µm, other species 39 –60 µm; differences signif-

icant at P = 0.05, Tukey test). Also, shade leaves of The upper epidermis had outer walls ranging from 5.5 to Umbellularia (39C5 µm) had significantly thinner palisade 7.7 µm on sun leaves, and from 4.3 to 6.1 µm on shade tissue than Q. chrysolepis, Chrysolepis chrysophylla, and leaves. The lower epidermis had outer walls ranging from Arbutus (Tukey test, P = 0.05). 4.2 to 6.6 µm on sun leaves and from 3.5 to 5.1 µmon Interspecific differences in the thickness of photosyn- shade leaves. thetic tissues often were not paralleled by differences in leaf Differences between sun and shade leaves also were specific weights (Table 1). For example, sun leaves of similar among the species. All species produced leaves of Arbutus menziesii had a 50% thicker palisade tissue than less area in sun than in shade (Fig. 1; t-test P = 0.05 except Q. chrysolepis, yet their specific weights were not signif- for Lithocarpus where P = 0.10). For all species, the sun icantly different and shade leaves of Q. chrysolepis had a leaves had a significantly thicker mesophyll with a thicker significantly higher specific weight and a significantly palisade tissue than the shade leaves (Table 1; t-test, thinner palisade tissue than shade leaves of Arbutus. All P = 0.05). species had similar shade leaf specific weights, but sun leaf However, species differed substantially in leaf size and specific weights had a wider range (Table 1). For shade

in the thickness of mesophyll tissues (Fig. 1, Table 1). leaves, only Q. chrysolepis had a significantly higher

Arbutus leaves were larger than those of other species (ave. specific weight (13.0C1.7 mg/cm2) and Umbellularia a 35.9 cm2 sun, 55.7 cm2 shade). The leaves of Chrysolepis, significantly lower specific weight (8.5C1.3 mg/cm2) than Lithocarpus, and Umbellularia had average sizes ranging the other species (10.0–11.0 mg/cm2; Tukey test, P = 0.05). from 10.3–16 cm2, but still larger than those of both The specific weight of sun leaves ranged from Arbutus’s Quercus species (4.2 –9.1mcm2). 18.3 mg/cm2 to Umbellularia’s 13.8 mg/cm2, with specific

Table 1mMesophyll properties and specific weights for sun and shade mesophyll (n = 9); P Layers = number of palisade parenchyma layers saplings of six broadleaf evergreen tree species at the Northern (n = 9); LSW = Leaf specific weight (n = 90); BSW = Branch Specific

California Coast Range Preserve in Mendocino County, California. Weight – mass of a new branch segment per cm2 of leaf area supported (Mesophyll = thickness of all mesophyll – spongy mesophyll plus (n = 18). Values are means C SD) palisade parenchyma (n = 9); Palisade = thickness of palisade layers of

Species Mesophyll Palisade P Layers LSW BSW (µm) (µm) (number) (mg/cm2) (mg/cm2)

Sun leaves

C C C C Arbutus menziesii 271C55 151 47 2.7 0.5 18.3 3.0 3.0 0.9

C C C C Chrysolepis chrysophylla 215C34 113 18 2.9 0.3 16.7 3.6 3.8 0.4

C C C C Lithocarpus densiflorus 189C19 76 5 2.0 0.0 15.1 2.5 3.0 0.9

C C C C Quercus chrysolepis 209C18 97 20 2.4 0.5 17.4 2.3 6.5 3.1

C C C C Quercus wislizenii 239C64 122 35 2.3 0.5 16.0 2.9 5.9 2.2

C C C C Umbellularia californica 190C10 80 9 2.0 0.0 13.8 4.2 1.8 0.7

Shade leaves

C C C C Arbutus menziesii 202C19 74 14 2.0 0.0 10.9 1.5 1.9 0.8

C C C C Chrysolepis chrysophylla 149C22 58 13 1.9 0.3 11.0 1.5 2.7 0.5

C C C C Lithocarpus densiflorus 127C48 48 10 1.6 0.3 10.0 1.1 2.1 0.7

C C C C Quercus chrysolepis 149C 8605 2.0 0.0 13.0 1.7 3.5 1.1

C C C C Quercus wislizenii 127C 7518 1.7 0.5 10.6 1.8 3.0 1.4

C C C C Umbellularia californica 145C22 39 5 1.0 0.0 8.5 1.3 1.1 0.3 172 Table 2mLeaf anatomical traits for the six species of broadleaf ever- green trees growing at the Northern California Coast Range Preserve, Mendocino County, California. Based on observations of sections of leaves from six saplings of each species. (Presence of a trait denoted by a 1. Species: AM = Arbutus menziesii, CC = Chrysolepis chrysophylla, LD = Lithocarpus densiflorus, QC = Quercus chrysolepis, QW = Quercus wislizenii, UC = Umbellularia californica. Traits: B. S. Extensions = Sclerophyllous bundle sheath extensions from vein to epidermis; D. Crystals = Druze crystals in mesophyll; E. Deposits = Epicuticular deposits on lower epidermis; Hypo- dermis = Hypodermis below upper epidermis; S. Idioblasts = Secretory idioblasts in mesophyll; Trichomes = Trichomes on lower epidermis) Trait AM CC LD QC QW UC B. S. Extensions 1 1 1 1 1 1 D. Crystals 0 1 1 1 1 0 E. Deposits 0 1 1 1 0–1a 0 Hypodermis 0 0 1 0 0 0 S. Idioblasts 0 0 0 0 0 1 Trichomes 0 1 0–1b 000 aThin, discontinuous and occasionally absent b Scattered, mostly near major veins

tissues in that volume, the efficiency of displaying photo- synthetic tissues, and the longevity of leaves differed among species. Interspecific differences in volume occupied by a branch Fig. 2mBranch volume and leaves per cm branch for sun and shade (Fig. 2) were due to leaf size and shape, because there were saplings of six broadleaf evergreen tree species at the Northern no interspecific differences in length of branch extension. California Coast Range Preserve in Mendocino County, California. [Volume = volume of space occupied by current branch segment and The branches of Q. chrysolepis and Q. wislizenii, having

leaves; Leaves/Branch Length = number of leaves per cm of branch smaller leaves, occupied 1/3–1/13th less space (sun

C C length for current branch segment. AM = Arbutus menziesii, CC = 170C120 and 316 167 cm3, shade 261 140 and Chrysolepis chrysophylla, LD = Lithocarpus densiflorus, QC = 347C272 cm3 respectively) than did other species (sun

Quercus chrysolepis, QW = Quercus wislizenii, UC = Umbellularia 707–2172 cm3, shade 1094–2304 cm3). californica. Values are means C 1SE(n= 18)] Except for Chrysolepis, all species branches explored similar volumes in sun and shade (t-test, P = 0.05). How- ever, all but Arbutus and Q. wislizenii spaced leaves further

2 weights R1.3 mg/cm apart being significantly different apart on shade branches than on sun branches (Fig. 2), (Tukey test, P = 0.05). reducing crown mass and total leaf area in shade. The shade The lack of correspondence between photosynthetic branches of all species except Arbutus had significantly less tissue thickness and leaf specific weight was due to inter- crown mass per volume (leaf plus branch mass/volume) specific differences in leaf anatomy. Qualitative differences than did sun branches (Fig. 3) and, despite increases in between species included the presence or absence of average leaf area, all species except Q. wislizenii had epicuticular deposits, hairs, crystals, secretory idioblasts significantly less leaf area per volume along shade branches and a hypodermis (Table 2). There also were quantitative than along sun branches (Fig. 3; t-test, P = 0.05). differences in anatomy besides mesophyll thickness. For In both sun and shade, Arbutus and both Quercus species example, the epicuticular deposits of Lithocarpus were as had significantly more leaf area per volume than did thick as the outer epidermal wall, those of Chrysolepis and Chrysolepis, Lithocarpus, and Umbellularia (Fig. 3; Q. chrysolepis were thinner, and the epicuticular deposits of Tukey test P = 0.05). Arbutus and both Quercus species Q. wislizenii. were thin, discontinuous and often absent. also had significantly more crown mass per volume along Similarly, the sclerophyllous bundle sheath extensions were branches (Fig. 3; Tukey test P = 0.05) and a greater volume most pronounced in Q. chrysolepis and least so in Umbel- of palisade parenchyma per volume of space along lularia. These anatomical differences all influence leaf branches (Fig. 3). specific weight separately from mesophyll thickness. Though Quercus species had more leaf tissue per vo- lume, they did not have a more efficient display of photo- synthetic tissue. These smaller-leaved species had more Branch architecture branch mass per leaf area (Table 1; Tukey test P = 0.05), and their crown mass per volume of palisade tissue was Species differed substantially in the distribution of photo- comparable to or higher than that of other species (Fig. 4). synthetic tissue on both sun and shade branches. Volume In sun, Q. chrysolepis had significantly higher crown mass occupied by a branch, the concentration of photosynthetic per palisade volume than all species but Lithocarpus (Fig. 4; 173

Fig. 4mCrown mass per volume of palisade parenchyma for sun and shade branches of broadleaf evergreen tree species at the Northern California Coast Range Preserve, Mendocino County California. [AM = Arbutus menziesii, CC = Chrysolepis chrysophylla, LD = Lithocarpus densiflorus, QC = Quercus chrysolepis, QW = Quercus wislizenii, UC = Umbellularia californica. Error bars represent 1 SE (n = 18)]

wislizenii also had primarily a single cohort per branch

C (average 1C0 and 1.2 0.3, respectively). Saplings of the other species had multiple cohorts per branch in both sun

and shade, though less in sun than shade (Chrysolepis

C C 3.6C1.3 sun and 5.5 1.3 shade, Lithocarpus 3.9 1.6

C C and 6.0C2.0, Q. chrysolepis 2.6 1.0 and 3.9 1.1, Um-

C

bellularia 2.7C0.8 and 5.4 1.1) his™ussion

Crown attributes are part of the suite of traits determining a species’ environmental tolerances and allowing relatively greater growth than other species under particular combina- tions of light, water, nutrients, and temperature (Horn 1971; Givnish 1979, 1988; Nobel 1983; Harper 1985; Ku¨ppers Fig. 3mCrown mass, leaf area, and palisade tissue per volume for sun 1989). From that perspective, these trees all possess crown and shade branches of broadleaf evergreen tree species at the Northern attributes, like thick epidermal walls and the evergreen California Coast Range Preserve, Mendocino County. [Crown mass/ habit, that allow their persistence in California’s relatively Volume = mass of leaves and branch in most recent branch segment equable but seasonally arid climate. Despite these com- divided by volume occupied by branch segment and leaves; Leaf Area/ monalities, however, differences in branch architecture, leaf Volume = leaf area of most recent branch segment divided by volume occupied by branch segment and leaves; Palisade tissue/Volume = longevity, and leaf area divide the species into groups that volume of palisade tissue in most recent branch segment’s leaves correspond to habitat distinctions and individual species divided by volume occupied by branch segment and leaves. AM = distributions. Arbutus menziesii, CC = Chrysolepis chrysophylla, LD = Lithocarpus Chrysolepis, Lithocarpus, and Umbellularia all had a densiflorus, QC = Quercus chrysolepis, QW = Quercus wislizenii, UC = Umbellularia californica. Error bars represent 1 SE (n = 18)] lower density of photosynthetic tissue per volume and a slower turnover in foliage. Both traits may contribute to the greater shade tolerance these species display relative to Arbutus and Quercus. Tukey test P = 0.05). In contrast, Arbutus had significantly Shade-tolerant species generally concentrate less leaf less mass per palisade volume than all species in shade, and mass per volume (Ku¨ppers 1985; Canham 1988). This less than Lithocarpus, Q. chrysolepis, and Q. wislizenii in increases support costs but reduces self-shading and allows sun. a greater exploration of space and a greater increase in Species differed in leaf longevity. Crowns of fallen crown volume per unit increase in mass. canopy trees of Arbutus and Q. wislizenii rarely had two A slow rate of leaf turnover also may contribute to shade cohorts of leaves on a branch, whereas those of tolerance (Baker 1934; Chabot and Hicks 1982; Bongers Chrysolepis, Lithocarpus, and Umbellularia had up to and Popma 1990; Reich et al. 1992; Gower et al. 1993). nine cohorts and retained most leaves in the four youngest Understory seedlings of these species often produce no new cohorts. Both sun and shade saplings of Arbutus and Q. foliage or lose foliage to browse herbivory (personal 174

observation; Hunter 1994). In these situations, older foliage allows persistence of the individual. Furthermore, if older ‚eferen™es foliage makes a significant contribution to carbon gain, Baker FS (1934) Theory and practice of silviculture. McGraw-Hill, then extended leaf longevity amortizes the cost of leaf New York construction over a longer period. This may be the case Barbour MG, Major J (1977) Introduction. In: Barbour MG, Major J for these species: Field et al. (1983) examined four cohorts (eds) Terrestrial vegetation of California. California Native Plant of leaves on Umbellularia saplings and found no significant Society, Sacramento, pp 3–11 Bongers F, Popma J (1990) Leaf dynamics of seedlings of rain forest relationship between leaf age and photosynthetic capacity. species in relation to canopy gaps. 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Denser display of foliage has been interpreted as ecological study of the chaparral and its related communities. requiring less support tissue and allowing more rapid Publication No. 319, Carnegie Institution of Washington, Washing- ton, D.C. growth (White 1983; Canham 1988; Ku¨ppers 1989), and Dale VH, Hemstrom M (1984) CLIMACS: a computer model of forest more rapid leaf turnover is often associated with higher stand development for western Oregon and Washington. Research relative growth rates (Reich et al. 1992; Gower et al. 1993). Paper PNW-327, U.S. Forest Service, Department of Agriculture, These generalizations seem to apply to Arbutus, whose Portland Duhme F, Hinckley TM (1992) Daily and seasonal variations in water large leaves are closely packed and have a thick palisade relations of macchia shrubs in France (Montpellier) and Turkey tissue, resulting in a lower mass of leaves and branches per (Antalia). Vegetatio 99–100: 185–198 volume of palisade tissue. 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In: Jackson JBC, Buss LW, Cook RE (eds) Population biology and evaluated through future studies combining ecophysiologi- evolution of clonal organisms. Yale University Press, New Haven, cal and modeling approaches. pp 1–34 In general, determining the functional significance of Hickman JC (ed) (1993) The Jepson manual: higher plants of Cali- morphological traits is important, particularly for ecosys- fornia. University of California Press, Berkeley Horn HS (1971) The adaptive geometry of trees. Monographs in tem modelers and others grouping species on the basis of Population Biology 3. Princeton University Press, Princeton functional similarities. For example, physiological studies Hunter JC (1994) Differential browsing by deer upon understory of sclerophylls reveal both a wide range in resource use and saplings of five tree species in coastal California’s forests. 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