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Ecology |
2Department of Biology, University of California, Riverside, California 92521 USA; 3Department of Entomology, University of California, Riverside, California 92521 USA
Received for publication December 13, 2001. Accepted for publication April 9, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Asteraceae • environmental gradient • growth rate • herbivory • heritability • leaf pubescence • local adaptation • phenotypic plasticity • plant architecture • Trirhabda geminata
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Harper, 1989
). The size and shape of an individual plant hence is thought to reflect both a genetically determined developmental program, as well as effects of the environment on resource acquisition and growth rates.
Much progress in understanding the basis for growth form variation has been made using a variety of approaches. Computer simulations have demonstrated that algorithms for modular accretion can mimic a variety of growth forms (Room, Maillette, and Hanan, 1994
). Both genetic and environmental effects on various aspects of plant morphology have been amply demonstrated in the field and through common-garden and transplant experiments (Turesson, 1922a
, b
; Clausen, Keck, and Hiesey, 1940
; Waser and Price, 1985
; Monson et al., 1992
; Sandquist and Ehleringer, 1998
). Cross-environment comparisons have revealed the adaptive nature of such characters as plastic stem-elongation responses to light level (Schmitt, 1997
), overall stature and allocation to root, stem, and canopy (Tilman, 1982
; Gleeson and Tilman, 1994
), leaf size and shape (Orians and Solbrig, 1977
; Ehleringer and Cook, 1990
), and root morphology (Peterson, 1992
; Kerley, 2000
). Cross-species comparisons have revealed allometric patterns suggestive of mechanical design constraints (Corner, 1949
; Ackerly and Donoghue, 1998
).
Despite this progress, in relatively few cases do we have detailed understanding of how plant architecture is produced by the interplay between a genetically determined developmental program and a plant's physiological response to its growth environment. Employing a common garden approach, we explored how genetic and plastic variation in leaf characters affect growth and architecture in a desert shrub, Encelia farinosa.
The study system
Encelia farinosa Gray ex. Torr. (Asteraceae), or brittlebush, is a small perennial shrub (height 3–15 dm) whose range extends from the inland valleys of southern California (Sawyer and Keeler-Wolf, 1995
) to low-elevation Mojave and Sonoran Desert habitats of Nevada, Utah, Arizona, and Mexico (Clark, 1993
; Turner, Bowers, and Burgess, 1995
; Fig. 1). The species consists of three varieties (var. farinosa, phenicodonta, and radians) differentiated by flower color and/or leaf morphology (Shreve and Wiggins, 1964
). Maximum longevity has been measured at 30–50 yr, although most individuals live less than 7 yr (Goldberg and Turner, 1986
; Turner, 1990
).
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; Cunningham and Strain, 1969
). During periods of drought the plant sheds leaves and becomes dormant (Shreve, 1924
; Turner, Bowers, and Burgess, 1995
). Following sufficient rains, new leaves are initiated at distal tips of elongating shoots. As shoot growth slows, apical dominance weakens, and lateral shoots begin to develop from leaf axils, first at the base of actively growing shoots and then progressively more proximally along the branch. Some terminal shoots give rise to a paniculate inflorescence towards the end of the growing season. Plants typically drop their leaves and become dormant after flowering. When growth resumes after the onset of rain, 2–3 shoot meristems subtending last season's inflorescence begin to elongate rapidly, causing each flowering stem to branch; vegetative shoots may or may not branch, depending on the extent of lateral meristem development during the previous season.
Encelia farinosa exhibits considerable variation in leaf characters at a variety of scales. Individual plants produce leaves of differing size and pubescence in response to seasonal drought (Cunningham and Strain, 1969
; Smith and Nobel, 1978
). The first leaves produced after onset of rains are relatively large and glabrous and subsequently are smaller and more pubescent as water availability declines (Smith, Monson, and Anderson, 1997
). Individuals within populations vary in these same characters (Ehleringer and Mooney, 1978
). In addition, populations of E. farinosa that occupy hot, arid environments produce smaller and/or more pubescent leaves (Ehleringer and Mooney, 1978
; Ehleringer, 1983
; Sandquist and Ehleringer, 1997
, 1998
).
These population-level differences in leaf characters persist when plants are grown in common environments, suggesting a genetic basis (Ehleringer and Cook, 1990
; Sandquist and Ehleringer, 1997
; Housman, 1998
), and they appear to be adaptive (Ehleringer and Mooney, 1978
). Under sunny, dry conditions, small leaves are advantageous because they do not overheat when stomata close in response to water stress (Gates, 1965
). Pubescent leaves also maintain lower leaf temperatures and transpiration rates by reflecting incident solar radiation, but at the cost of lower maximum photosynthetic rates (Ehleringer and Mooney, 1978
; Smith and Nobel, 1978
). Under drought conditions, low transpiration rates can extend the period during which stomata remain open and active photosynthesis can occur (Sandquist and Ehleringer, 1997
, 1998
).
Specific predictions
The extensive previous ecophysiological work on E. farinosa establishes that leaf size and pubescence interact with water availability and intensity of solar radiation to determine seasonal growth. Variation in seasonal growth associated with leaf characters in turn can be expected to have a secondary influence on growth form of woody species like E. farinosa, because branch length and branching patterns reflect cumulative growth history (Valladares, 1999
). If growth rates are high and/or the growing season is prolonged, interbranch distances will be large, and plants will have a sprawling growth form. If growth rates are low and/or drought truncates the growing season, interbranch distances will be small and plants will have a compact, branching growth form. We evaluated this expected link between leaf characters and plant architecture by testing three specific predictions: (1) E. farinosa populations inhabiting hot, dry localities have smaller and more pubescent leaves, are more branched, and display a more compact growth form than populations inhabiting more mesic environments. (2) Interpopulation differences in leaf characters and growth form persist in offspring grown in common gardens to the extent that they are genetically determined. (3) Offspring grown in garden environments similar to their home environments will outperform offspring from other environments to the extent that there is local adaptation. We tested these predictions by measuring morphology of E. farinosa plants growing naturally across a temperature and moisture gradient and by measuring their offspring grown in common gardens that reflect a similar gradient.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The two "desert" populations, Cadiz (34°32'07'' N, 115°28'34'' W, approximately 330 m asl, San Bernardino County, California, USA) and Mohawk (32°43'42'' N, 113°44'23'' W, approximately 152 m asl, Yuma County, Arizona, USA) occur in Mojave and Sonoran desert-scrub vegetation, respectively. Our study populations lay outside the range of E. farinosa var. radians and contained few if any purple-disked individuals. Hence, our study populations were predominantly E. farinosa var. farinosa.
Seed collection and germination
In April and May 1995, we collected 2–4 flower heads containing mature achenes from each of 10–11 haphazardly chosen plants in each of the four source populations (6000 mature seeds, with 77–351 seeds per family). Because E. farinosa is an obligate outcrosser (Ehleringer and Clark, 1988
), seeds collected on one plant are members of maternal full- to half-sib families.
On 1 April 1996 seeds were soaked for 1 h in a 0.01 mg/mL gibberellin solution to increase germination success (Foley, 1992
; Taiz and Zeiger, 1998
) and then sprinkled evenly into 20 x 10 x 10 cm aluminum pans filled with moist vermiculite (one pan per family). The pans were kept on plastic trays in a greenhouse at UCR that tracked ambient conditions, and were watered every 3–4 d. After 1 mo, we individually transplanted 620 seedlings from 41 families into 10 x 10 cm plastic pots filled with Uni-Gro Cactus Mix (L & L Nursery Supply, Chino, California, USA). Pots were watered twice weekly and rotated monthly to minimize the effect of any environmental heterogeneity within the greenhouse.
Common gardens
In October 1996, we randomly chose half the surviving plants from each family to be transplanted either into a common garden at the Agricultural Experiment Station (hereafter AES) at UCR (33°57'40'' N, 117°19'58'' W, approximately 311 m asl) or into a common garden approximately 80 km inland at the Living Desert Museum (hereafter LD) in Palm Desert (33°42'28'' N, 116°22'10'' W, approximately 104 m asl, Riverside County, California; Fig. 1). The transplants were spaced 0.5 m apart in an 8 x 7.5 m plot, with individuals from each population represented in each row and column. To reduce transplant shock, we covered gardens with 60% shade cloth for the first 2 wk after transplanting. Each transplant received 1 L of water twice per week for the first month, and no supplemental water thereafter. Early mortality was minimal and did not differ significantly among populations. The AES garden contained 216 plants from eight, ten, nine, and ten families from the Cadiz, Mohawk, Spruce, and UCR source populations, respectively. The LD garden contained 210 plants representing five, ten, nine, and ten families from the aforementioned source populations, respectively.
Climate
Thirty-year records (National Climatic Data Center, 1961–1990; http://www.ncolc.noaa.gov) indicate that the two coastal populations experience temperatures that average 3.0°C cooler than the two desert populations. On average, Cadiz and Mohawk populations receive 5.3 cm and 10.6 cm precipitation in the cool season (October–March), respectively, and 5.5 cm and 11.1 cm precipitation in the warm season (April–September). Coastal populations receive 21.1 cm precipitation on average in the cool season and 4.3 cm precipitation in the warm season.
Compared to the 30-yr average, plants in both experimental gardens experienced above-average temperatures and below-average precipitation during this study (September 1996–June 1997; AES, 1.4°C higher, 4.4 cm lower; LD, 1.5°C higher, 8.5 cm lower). These deviations resulted in relatively short growing seasons for both coastal and desert gardens and a coastal garden environment somewhat more typical of the climatic conditions encountered in the desert.
Morphometric measurements
Between late March and early April 1997 we measured leaf, growth form, and size variables for plants growing in source populations. From February to May 1997, when the plants were 11–14 mo old, we measured these traits on plants in the common gardens. The same trait was always measured in both common gardens within the period of 1 wk. Additionally, groups of similar traits (e.g., leaf length, width, and pubescence) were measured at the same time on individual plants.
Plant size was measured as height, canopy diameter, maximum lateral shoot length, total leaf number, and (for offspring in common gardens) total dry mass (Fig. 2). Height was the vertical distance from the soil surface to the tip of the tallest shoot. Canopy diameter was calculated as the mean of the maximum diameter and the diameter perpendicular to the maximum. The longest lateral shoot was estimated as the maximum linear distance from a terminal meristem to the junction of the shoot and the basal plant stem. Leaf number was the total number of photosynthetically active leaves large enough to have a clearly visible petiole. At the end of the growing season, we excavated a subset of plants from each garden, cleaned roots of soil, separated roots from shoots, and dried them to a constant mass. Allocation to above- vs. belowground structures was estimated as the dry root mass/total dry mass.
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We also measured leaf variables including length, width, and pubescence. Leaf length and width were measured to the nearest millimeter on the largest leaf on each plant. Leaf pubescence was estimated indirectly by matching the top surface of the largest leaf to a paint swatch. To convert swatch colors to an index of leaf reflectance, black and white photos were taken of the paint swatches next to a gray scale that was constructed following the methods of Kevan et al. (1973)
. Index values ranged from 1 to 14, with greater values indicating greater pubescence and reflectivity.
Herbivory
Encelia farinosa is attacked primarily by the specialist beetle, Trirhabda geminata Horn (Wisdom, 1985
). To assay herbivore damage on each plant, we counted the fraction of leaves with herbivore damage and estimated overall leaf herbivory using a 1–6 scale (1 = no herbivory, 2 = 1–10% of leaf area removed, 3 = 11–20%, 4 = 21–30%, 5 = 31–40%, and 6 = 41–50%).
Statistical analyses
All statistical analyses were performed using the GLM and DISCRIM procedures of SAS (SAS Institute, 1989
). We performed separate analyses on leaf, growth form, size, and herbivory variables. We first used univariate (ANOVA) and multivariate (MANOVA) analysis of variance to assess the significance of variation among source populations, testing source environment effects over population nested within environment as an error term for univariate analyses and, due to limited degrees of freedom, over the error sums of squares and cross products matrix for multivariate analyses. We then used canonical discriminant analysis to describe the patterns of variation among the four source populations and among offspring grown in each common garden.
We also used ANOVA and MANOVA to assess variation among offspring from different source environments and plastic responses to the two garden environments, using within-garden family mean values for all characters. In these analyses we treated garden (AES or LD), source environment (coastal or desert), and garden x source environment as fixed effects and family within environment as a random effect. Environment was tested using family within environment as the error term. All other effects were tested using the interaction between family and garden as the error term. To determine whether there was variation among families within gardens, we conducted separate analyses by garden, using data from individual plants, and tested family effects using individual within family as the error term. To assess the extent to which offspring resembled their parental population, we calculated offspring scores on the canonical discriminant functions that best described variation among parental populations and correlated offspring with parental scores.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant size differed significantly between desert and coastal offspring (Wilks' lambda = 0.51, F5,30 = 5.75, P = 0.0008) and between gardens (Wilks' lambda = 0.04, F5,20 = 97.88, P = 0.0001). Contrary to patterns among source populations, desert offspring were larger or equal in size to coastal offspring in both gardens in all size measures except for total leaf number (Table 4). They also allocated proportionally less to root biomass (F1,34 = 50.39, P = 0.0001; Table 4). Plants growing in the coastal garden also allocated proportionally less to root biomass than did plants growing in the desert garden (F1,24 = 37.15, P = 0.0001; Table 4). No individuals flowered in the desert garden, whereas some flowered in the coastal garden (Table 4).
Herbivory (Wilks' lambda = 0.15, F3,29 = 56.05, P = 0.0001) differed significantly between gardens, but not between desert and coastal offspring within a garden (Table 4). Relative to the desert garden, all families grown in the coastal garden experienced greater levels of herbivory (Table 4).
Significant environment x garden interactions indicate that the strength of plastic responses in the common gardens differed for families from coastal and desert populations for leaf characters (Wilks' lambda = 0.51, F3,29 = 9.39, P = 0.0002), plant growth form (Wilks' lambda = 0.34, F2,30 = 28.69, P = 0.0001), and plant size (Wilks' lambda = 0.23, F5,20 = 24.81, P = 0.0001). Leaf size was more plastic, and pubescence less plastic for coastal than for desert families. Shoot number changed less and first branch distance changed more for families from coastal environments. Plant size changed more between gardens, but total leaf number changed less, for coastal than desert families (Table 4).
Although all families had lower growth rates and failed to flower in the desert garden, desert offspring outperformed coastal offspring in terms of biomass accumulation. However, offspring from coastal source populations did not outperform desert offspring in the coastal garden. Coastal offspring produced equivalent total biomass but fewer inflorescences than desert offspring in the coastal garden (F1,35 = 16.51, P = 0.0003; Table 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1998
) that Encelia farinosa populations occupying hot, dry environments produce smaller, more pubescent leaves than populations in more mesic environments. These differences were maintained in offspring grown from seed in common gardens, indicating that leaf characters are heritable (Clausen, Keck, and Hiesey, 1940
; Langlet, 1971
; Ehleringer, 1983
; Gurevitch, 1992
; Sandquist and Ehleringer, 1998
). Plastic responses consistent with previous reports of seasonal variation in leaf characters (Cunningham and Strain, 1969
; Ehleringer and Mooney, 1978
) were also evident; all families produced larger and less pubescent leaves in the coastal than the desert garden. The magnitude of plastic responses in several characters differed for desert and coastal populations. Coastal families showed greater between-garden responses in characters related to growth performance (e.g., leaf size and overall plant size), but were less plastic in leaf pubescence. One plausible explanation for the difference in leaf plasticity is that the coastal plants in western Riverside County typically experience morning fog in late spring, and this may shift the relative value of achieving water economy by way of a flexible stomatal response. Thus a better strategy along the coast might be adjusting conductance instead of pubescence with its attendant fixed cost in terms of maximum photosynthetic rate. The differences shown in plasticity of growth performance may reflect the relative effectiveness of alternative genetically determined strategies for achieving water economy in desert vs. coastal environments. Patterns of covariation between leaf characters and branching propensity confirm our expectation that plant architecture is influenced by seasonal growth rates. As expected, offspring from desert populations, which have more pubescent leaves and presumably therefore lower maximum photosynthetic rates, had greater branching propensities in both gardens than offspring from coastal populations. In addition, all offspring had a greater branching propensity in the desert, where there is a shorter period of moisture available for growth compared to coastal environments. Thus, architectural diversity within Encelia farinosa appears to result from a cumulative growth history that is determined by seasonal growth rate. Seasonal growth rate in turn is determined by leaf characters that affect photosynthetic rate and by the length of the period in which moisture is available for growth.
Patterns of overall growth and flowering of offspring in common gardens provide only partial support for our expectation of local adaptation. Whereas desert offspring outperformed coastal offspring in the desert garden by all measures, coastal offspring outperformed desert offspring in the coastal garden in leaf production, but not inflorescence production or overall size. This apparent discrepancy could be a consequence of the unusual weather patterns in both common garden sites during our study. The unusually warm and dry conditions may have resulted in the poor performance of coastal offspring. Different patterns would likely have been observed if measurements had been averaged over multiple seasons.
Stronger patterns may also have been observed if we had measured growth for a longer period after seedlings were transplanted into gardens. Desert offspring grew 1.46 times taller than coastal offspring in the greenhouse and hence displayed a considerable size advantage (by that measure) at the time they were transplanted into the common gardens (Housman, 1998
). This size advantage was maintained in the desert garden (where the ratio of desert : coastal offspring mass averaged 1.49; Table 4) but was greatly reduced in the coastal garden (to a ratio of 1.10). Coastal offspring therefore grew relatively more than desert offspring after being transplanted into the coastal environment. If we had observed cumulative growth over a longer period of time, coastal offspring may have eventually outperformed desert offspring because past research has shown that fitness differentials tend to increase with the fraction of the total life span observed (Waser and Price, 1994
).
Greater overall growth of desert offspring in the greenhouse may also reflect a less conservative growth response to warm-season precipitation, which occurs very infrequently in the Mediterranean climate of coastal California and increases to the east with increasing monsoonal influence (Ehleringer, 1994
; Sandquist and Ehleringer, 1997
). In our study, germinated seedlings were watered during their first summer of growth, and desert offspring responded with the greatest growth. It is possible that coastal genotypes maintained lower stomatal conductance and hence grew more slowly under the warm greenhouse conditions. Sandquist and Ehleringer (1997)
observed similar variation in stomatal response between E. farinosa populations having different average frequencies of spring precipitation.
A dramatic difference in herbivory occurs between coastal and desert populations, with up to 50% defoliation in some coastal individuals (Wisdom, 1985
; R. Redak, University of California, Riverside, personal observation) and no defoliation in the desert. Louda (1982)
also observed higher levels of herbivory in coastal populations of Asteraceae along a similar coastal/desert gradient. It is unclear why herbivory by T. geminata does not occur in the desert. Paine, Redak, and Trumble (1993)
found a preference in T. geminata for leaves exposed to acidic fogs typical of urban southern California, but the lack of a significant difference in herbivory for coastal and desert offspring in our coastal garden suggests T. geminata does not prefer local genotypes or avoid heavy pubescence that deters herbivores in some systems (Stipanovic, 1983
). Hence, leaf pubescence in E. farinosa does not appear to represent an anti-herbivore character with respect to the dominant insect herbivore for this species.
Our success in relating aspects of growth form to leaf characters that affect water-use efficiency and photosynthetic rate underscores the value of viewing plant architecture as the realization of a programmed pattern of growth given constraints imposed by a plant's physiological responses under a particular environmental context. Nonetheless, our observations to date are largely phenomenological, and it is unclear to what extent characters other than leaf size, shape, and pubescence affect overall plant size and shape. Plant growth represents an integrated response to both biotic and abiotic factors including competitors, pollinators, herbivores, climate, and soils. The variation we observed in greenhouse growth rates is suggestive of additional variation in physiological responses to warm- vs. cool-season moisture. Previous work (Ehleringer and Cook, 1990
; Sandquist and Ehleringer, 1996
, 1998
) suggests variation also exists, both within E. farinosa and between Encelia species, in such characters as initiation and shedding of leaves. Future exploration of the mechanistic pathways by which leaf size and pubescence affect growth rate and physiological responses will be needed to fully understand the basis for growth form variation in E. farinosa.
The phenotypic variation we observed in E. farinosa is reflected within the genus Encelia as a whole. Its 15 members have undergone adaptive radiation throughout the arid lands of southwestern North America and western South America, with each species becoming adapted to a different habitat (Ehleringer and Clark, 1988
). Encelia farinosa belongs to the californica clade, one of two major subdivisions of the genus, and has the largest geographic range of any species in this clade, encompassing the greatest variation in temperature and precipitation. Thus phenotypic differentiation within this single species, in response to variation in the physical environment, may serve as a model for understanding the proliferation of species within the clade.
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FOOTNOTES |
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4 Author for correspondence, present address: University of Nevada, Las Vegas, Department of Biological Sciences, 4505 Maryland Parkway, Las Vegas, Nevada 89154-4004 USA (housman{at}unlv.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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