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Ecology |
Biological Sciences, Stanford University, Stanford, California 94305 USA
Received for publication April 8, 2004. Accepted for publication December 1, 2004.
ABSTRACT
Many woody plant species that depend upon fire-cued seed germination lack the ability to resprout. As the ability to resprout is widely assumed to be the ancestral condition in most plant groups, the failure to sprout is an evolutionary derived trait. Models for the evolutionary loss of sprouting assume a trade-off between seedling success and vegetative resprouting ability of adults. Such models require higher seedling success rates in nonsprouters than in sprouters. On the other hand, there seem to be few a priori reasons why a strong sprouter might not also have highly competitive post-fire seedlings. To test the hypothesis that nonsprouting plants have higher growth rates and/or drought survival, we grew seedlings of Ceanothus tomentosus from sprouting and nonsprouting populations in a common garden experiment. Each of these C. tomentosus populations was paired with a sympatric Ceanothus species that differed in resprouting ability. Sprouters exhibited greater allocation to root carbohydrate storage than did nonsprouters, but overall relative growth rates did not differ. Nonsprouters had earlier onset of flowering. These results provide mixed support for models of a sprouting/nonsprouting allocation trade-off.
Key Words: allocation • carbon storage • fire • iteroparity • nonsprouters • sprouters
Some woody species that are dependent upon fire to cue seed germination have apparently lost the ability to resprout following fire. The ability to resprout is widely assumed to be the ancestral condition in most plant groups, whereas loss of ability to resprout is the derived condition (Wells, 1969
; Bond and Midgley, 2003
). The loss of resprouting represents a significant demographic cost, as adults are killed by fire. Theoretical models for the evolution of nonsprouting (analogous to the evolution of semelparity from iteroparity) require some demographic advantage to offset this cost (Charnov and Shaffer, 1973
; Bond and van Wilgen, 1996
). The relative fitness of a resprouting life history has been modelled as a trade-off between sexual and vegetative allocation (Keeley and Zedler, 1977
; Hilbert, 1987
; Bellingham, 2000
), and has often been assumed to reflect a cost associated with allocation of resources to storage (Bond and Midgley, 2001
).
The hypothesized allocation cost associated with investing in resprouting structures could manifest at different points in the plant's life cycle. Studies in Australia have found greater root starch storage in sprouter adults than in nonsprouters, but higher growth rates among nonsprouters (Pate et al., 1990
; Bell and Pate, 1996
; Bell and Ojeda, 1999
; Bell, 2001
). The evidence for fecundity differences, however, is mixed. Some studies have found either no fecundity differences or greater yearly fecundity for sprouters: e.g., South African Erica (Bell and Ojeda, 1999
), Australian Banksia and Leucospermum (Lamont, 1985
; Zammit and Westoby, 1987
), and California Arctostaphylos (Keeley, 1977
; Keeley and Zedler, 1977
; Kelly and Parker, 1990
) and Ceanothus (S. Davis, Pepperdine University, personal communication). Other studies, however, have found allocation differences, suggesting a fecundity trade-off with higher fecundity in nonsprouters: e.g., Ceanothus (Keeley, 1977
; Carpenter and Recher, 1979
) and Hakea (Enright and Goldblum, 1999
).
The lack of a clear tradeoff between resprouting ability and fecundity has promped some researches to investigate seedling survival differences between sprouters and nonsprouters. Empirical evidence of greater seedling drought survival among nonsprouters (Frazer and Davis, 1988
; Thomas and Davis, 1989
; Pratt et al., 1997
; Williams et al., 1997
) suggests that a sprouter vs. nonsprouter trade-off may result from differential seedling competitive ability, especially during drought. Allocation tradeoffs could lead to competitive differences between seedlings of sprouters and nonsprouters only if allocation differences appear early in ontogeny. Although the field studies cited earlier suggest a differential seedling growth and survivorship between sprouters and nonsprouters, it is difficult to explain why a seedling from a sprouter species should necessarily be a poorer performer, especially if the resprouter seedling begins allocating resources to underground carbohydrate storage only after the difficult establishment stage is accomplished.
Unlike fire-surviving sprouters, which invest in thick bark or underground storage organs, nonsprouters depend completely upon seedling regeneration following fire. There is reason to believe that competitive differences among chaparral species might result from different seedling growth rates and/ or drought tolerance. Shallow-rooted seedlings are especially vulnerable to water stress during the summer drought (Kummerow et al., 1981
; Poole et al., 1981
; Williams et al., 1997
; Davis et al., 1998
), and selective pressures may be greater during the first summer drought after wildfire than at any other stage (Keeley and Keeley, 1977
; Frazer and Davis, 1988
; Williams et al., 1997
). Some evidence suggests that species within the genus Ceanothus exhibit consistent differences in xylem vulnerability; species in the exclusively nonsprouting clade, subgenus Cerastes, have shallower roots and more resistant xylem than do members of subgenus Ceanothus (Davis et al., 1999
).
Because direct evidence of a trade-off between seed production and resprouting ability is mixed, we investigate the possibility that early seedling drought tolerance may provide a sprouter/nonsprouter demographic trade-off. The extensive field studies of Pate et al. (1990
, 1991
), Bell and Pate (1996)
, and Bell and Ojeda (1999)
have revealed striking differences between sprouter and nonsprouter root : shoot allocation. Differences among study site environmental conditions, however, can confound field comparisons of sprouters and nonsprouters from different locations. To our knowledge, only one study has compared sprouter and nonsprouter growth in a common garden; Jaks (1984)
compared a single species each from two different genera. No study has investigated the relationship between resprouting, growth rate, and drought tolerance in chaparral plants in a controlled garden experiment, nor has any study attempted an experimental design with both environmental and phylogenetic controls.
One difficulty with cross-species comparisons is finding closely related taxa that differ in the trait of interest. The chaparral genus Ceanothus contains both resprouting and nonsprouting species, and many chaparral communities have more than one species of Ceanothus. Sprouter–nonsprouter pairs within a community have been used for comparisons in ecological studies (e.g., Keeley, 1977
; Davis et al., 1998
). Such comparisons, however, are weakened by the phylogenetic distance between the resprouting and nonsprouting species—a species pair usually contains members of two distinct clades within the genus. These two well-supported clades (Hardig et al., 2000
) have consistent morphological differences as well as differences in resprouting ability: subgenus Cerastes is comprised of only nonsprouting species, and subgenus Ceanothus contains mostly resprouting species and several nonsprouters (McMinn, 1939
).
In our study, we compare growth rates and non-structural carbohydrate storage of sprouting and nonsprouting Ceanothus taxa during the first summer drought following germination, controlling for both source environment and phylogeny. Although our study was not designed to test for fecundity trade-offs, we also measured time to first flowering as a rough estimate of early reproductive effort. Ceanothus tomentosus C. Parry is an excellent study organism for investigating the relationship between seedling traits and resprouting ability because the species includes both sprouting and nonsprouting populations. Northern California populations resprout (D. Schwilk, personal observation; McMinn, 1939
), whereas disjunct southern California populations are nonsprouters (J. Keeley, USGS Sequoia Kings Canyon National Park, personal communication; D. Schwilk, personal observation). This study compared seedlings from both populations grown in a common garden. The paired population approach provides a phylogenetic control to this experiment. However, because several hundred miles separate these populations, it would be useful to have a community or environment control as well. To control for different native environments, the experiment included additional Ceanothus species; collected at each of the C. tomentosus collection sites, with contrasting sprouting behavior. A nonsprouting Ceanothus species was collected from the northern California site, and a resprouting species was collected from the southern California site (Table 1).
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MATERIALS AND METHODS
Seed collection
We identified two sites for seed collection based on the species-selection criteria in the introduction. At the northern California site, resprouter C. tomentosus grew alongside nonsprouter C. cuneatus (Hook.) Nutt. The southern site provided nonsprouter C. tomentosus and sprouter C. leucodermis E. Greene (Table 1). All except C. cuneatus are members of the subgenus Ceanothus clade. This design provides two sprouter–nonsprouter comparisons within subgenus Ceanothus; one between the two C. tomentosus populations and the other between the sympatric Southern California C. tomentosus and C. leucodermis populations. Seeds were collected during June– July 1999 from 10–30 parent plants per population at each site. Seeds were randomly assigned to treatments and harvest blocks while evenly representing all mother plants.
Experimental design
The main experiment took place on the Stanford University campus (37°25.9' N, 122°11.0' W), Stanford, California, during February–November 2000, with limited measurements through May 2002. The experimental design was a blocked array of 432 plants (4 populations x 3 water treatments x 12 replicates x 3 harvests). Seeds from the four populations of plants were subjected to a heat treatment (60 s submersion in boiling water) followed by a 2-mo cold treatment, then germinated in flats. There were no differences in germination rates among the populations. After 2 wk in the greenhouse, the plants were transplanted into growing containers, which consisted of upright sections of PVC pipe (95 cm long x 20 cm diameter) that were fitted with a PVC cap at the bottom. The cap contained 10–15 1-cm-diameter holes to allow drainage. The tubes were filled to within 1 cm of the top with a 3 : 1 mixture of topsoil and sand on top of 4 cm of coarse gravel. The soil column was mechanically compacted to prevent settling after planting.
Because the germination of our different populations was synchronized, the seedlings germinated later in the year than they would in the field. The water treatments allowed us to extend the spring rains artificially; we then extended the drought with rainouts. The plants were fertilized once soon after establishment in the PVC tubes with 600 mL of 20–20–20 (N-P-K) solution (100 ppm N). The water treatments were applied through a drip irrigation system with separate pressure regulators for each of three randomized blocks. Within each block, the three treatments were applied using pressure-compensating drip emitters of different capacities, such that the water applied per unit time in the high water treatment was twice that of the medium water treatment, which in turn was twice that of the low water treatment. A removable rainout system of clear greenhouse plastic over a wire frame (Tufflite IV, Armin Plastics, 18901 E. Railroad St., City Of Industry, California, USA) allowed us to prevent any ambient precipitation from reaching the experimental plants, but it was deployed only when rain threatened. Throughout the season, the water levels were adjusted in tandem in an attempt to keep the soil in the low water treatment as dry as possible without killing the plants. Plants were watered every day through May, then once a week, then once every 2 wk. Beginning in July, all watering ceased and the rainouts were used when necessary through the fall to impose a complete drought. The total water additions through the spring extension (20 April–30 June) were 5, 10, and 20 cm for the low, medium, and high water treatments, respectively.
We measured soil moisture in 48 growing tubes using time domain reflectometry (TDR; Topp et al., 1980
). These measurements were made along a pair of vertically oriented stainless steel waveguides that extended to depths of 60 cm. We used preexisting calibration curves for sandstone soil (J. Dukes, personal communication; but see Field et al., 1997
) to convert readings from a cable tester (Tektronix 1502C, Beaverton, Oregon, USA) to estimates of soil volumetric water content.
Nondestructive measurements
We took a suite of nondestructive measurements at three times during the season: 16–18 May (census 1), 19–20 June (census 2), and 10–11 August (census 3). Measurements included: basal stem diameter, length of the main stem, number of leaves on the main stem, number of leaves on other branches, and length and width of three mature leaves.
Harvests
Two harvests of 144 plants each were conducted at the beginning and end of the summer drought: 17–23 July (harvest 1) and 13–20 October (harvest 2). These harvests provided the biomass estimates for relative growth analysis. Predawn water potential of each plant was measured with a pressure bomb apparatus (Soilmoisture Equipment, Goleta, California, USA) before harvesting. Aboveground biomass was divided into separate categories: leaves, main stem, and auxiliary stems. The soil column was removed intact and separated into three depth sections: 0–30 cm, 30–60 cm, and 60–90 cm. Roots were separated from soil by washing. Root biomass was measured separately for each depth range.
The final 144 plants were allowed to grow until mid-November with no additional water. At this time, stem and root samples were collected from 36 plants for analysis of total nonstructural carbohydrates. Collected tissue was immediately frozen in liquid nitrogen, and carbohydrate content was analyzed according to da Silveira et al. (1978)
. After the collections for total nonstructural carbohydrates were completed, the rainouts were removed and the remaining plants were allowed to continue growing under natural rainfall.
Time to first flowering
The remaining 108 plants were allowed to grow under ambient rainfall through May 2002. As a coarse measure of early reproductive output, plants that flowered in the third growing season (spring 2002) were recorded. Due to poor pollination and high seed abortion rates, seed production was very low and was not measured
Analysis
Multiple regression of the census 1 measurements against the harvest 1 biomass measurements allowed us to estimate time t = 0 biomass for those plants not harvested until the second harvest. We produced a separate regression model for each population and for aboveground (stem) and belowground biomass, resulting in eight linear models with stem diameter and length having the strongest weight in all models (model slopes were not homogenous among species). These models were used only for predicting biomass and the time of harvest 1. Growth analysis was then carried out by comparing the measured harvest 2 data with the estimated biomass of these plants at the first harvest. Abscised leaves were impossible to collect in this outdoor experiment. Therefore, the relative growth rate analysis uses total stem biomass in place of total above-ground biomass.
Our experimental design allowed analysis by three-way ANOVA with the factors resprouting behavior (two levels), site (two levels), and water treatment (three levels). To investigate covariance relationships within our data, we compared standardized major axis (SMA) slopes, calculated according to Warton and Weber (2002)
using a likelihood ratio method. Homogeneity of slopes was determined by permutation testing using the (S)MAT software by Daniel S. Falster, David I. Warton, and Ian J. Wright (available at http://www.bio.mq.edu.au/ecology/SMATR). For homogeneous slopes, differences in elevation were tested by Model II ANCOVA (ANOVA after rotating x and y around the SMA).
RESULTS
Water treatments had significant effects on soil moisture as measured by TDR and on predawn water potential (Fig. 1), but no difference in water potential was found among populations. Across all populations, sprouters had higher final root shoot ratios than did nonsprouters. Sprouters and nonsprouters had homogenous slopes (SMA slope = 1.195, r2 = 3.341). For a given total aboveground biomass, sprouters had greater root allocation (Fig. 2) indicated by significant differences in elevation (df = 1, F = 14.42, P < 0.001).
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Relative growth rate was dependent on site and treatment (Table 3). Northern California plants had higher relative growth rates than did southern plants, and greater water availability resulted in higher relative growth rates (Fig. 3). Although overall growth rates did not differ between sprouters and nonsprouters, sprouters showed a greater relative belowground growth rate for the same aboveground growth rate (Fig. 4). SMA slopes were homogeneous (slope = 1.118, sprouters r2 = 0.064, nonsprouters r2 = 0.82) and there was a significant effect of resprouting behavior, (df = 1, F = 6.45, P = 0.013).
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Reproductive output in third growing season
Significantly more nonsprouter than sprouter C. tomentosus flowered in spring of 2002 (G test, G = 6.3, P < 0.025, Table 5). The other two species displayed almost no second-year flowering. Southern C. tomentosus plants showed a slight trend to flower earlier in the season, but multiple censuses throughout the spring ensured that differences in within-season timing did not bias the enumeration of flowering individuals.
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This study is the first to detect an effect of resprouting strategy on carbohydrate storage in an intraspecific comparison. Although this study did not reveal the hypothesized trade-off between resprouting ability and seedling growth rate, it did reveal several differences in relative allocation to roots and shoots between sprouters and nonsprouters (Fig. 2). These differences do not suggest any poorer seedling performance in the resprouting populations, however. Sprouters, in fact, had similar overall growth rates to nonsprouters, but had higher root carbohydrate levels.
The high chaparral seedling mortality documented during the summer drought (Frazer and Davis, 1988
; Davis et al., 1998
) suggests that differences in first-season growth might explain a sprouter vs. nonsprouter trade-off. No such differences are evident from this study, however. Drought treatments in this study were not as severe as the drought experienced by seedlings under natural conditions: only the low water treatment plants reached predawn water potentials as negative as those measured in Ceanothus in nature (Davis et al., 1998
, 1999
, 2002
), and mortality in the field is much higher than in our experiment. Additionally, growth rate as measured in this experiment may not be an adequate proxy for seedling survival and performance. Even if seedlings survive by tolerating drought with little growth, however, these shrubs' long-term survival depends upon sinking roots deep enough to sustain tolerable water potentials through subsequent droughts. Those seedlings with more extensive roots should be best positioned to take advantage of the winter rain when it arrives.
Differential storage of nonstructural carbohydrates in roots proved to be the most striking difference between sprouter and nonsprouter populations. This difference was significant among the two C. tomentosus populations, and the difference in carbohydrate storage between the two southern California populations, C. leucodermis and C. tomentosus, demonstrates the same effect between co-occuring species in the same subgenus. Presumably, carbohydrate storage in roots provides the reserves necessary for resprouting after fire (Bowen and Pate, 1993
). Greater starch storage in adults of resprouting species has been reported for Western Australian Proteaceae (Pate et al., 1990
), Epacridaceae (Bell and Pate, 1996
), and Restionaceae (Pate et al., 1991
), and for South African Erica spp. (Bell and Ojeda, 1999
). When such studies have investigated seedlings, significantly higher root carbohydrate storage has been found even in first-year seedlings of resprouting species (Pate et al., 1990
; Bell and Pate, 1996
). If sprouters maintain higher carbon allocation to roots, reduced above-ground investment should result. No difference in aboveground or total growth was detected in this study, however.
Although this study was not designed to test fecundity differences, the earlier onset of flowering in nonsprouter populations of C. tomentosus relative to sprouter populations (Table 5) suggests that nonsprouters may be allocating carbon to early reproduction rather than root carbohydrate storage. The net effect of these two allocation strategies may result in no difference in growth rates between sprouters and nonsprouters, yet still represent a sprouter vs. nonsprouter trade-off between sexual and vegetative reproduction.
Differential carbon allocation is not the only possible explanation for the evolutionary loss of resprouting. Wiens et al. (1989a
, b
) have suggested that long-lived plants may accumulate somatic mutations that manifest in greater seed abortion and perhaps reduced seedling fitness. Meney et al. (1997)
found higher seed abortion rates among resprouting monocots, and recent work by Steve Davis and students (S. Davis, Pepperdine University, personal communication) suggests that resprouting chaparral shrubs may have much higher rates of spontaneous seed abortion than the nonsprouting species. This difference is hypothesized to result from accumulated somatic mutations in the long-lived resprouters. Our own preliminary measurements of seed abortion in C. tomentosus, however, revealed no difference in abortion rates between the northern and southern populations, although the northern (resprouting) population had higher rates of predation by parasitic wasps (unpublished data).
Another possible nonallocation difference between sprouters and nonsprouters is that nonsprouters have on average shorter generation times and potentially increased rates of evolution. In a changing environment, lineages with short generation times may have an advantage (e.g., Schwilk and Kerr, 2002
). Short generation time has been proposed as an explanation for the seemingly high rates of speciation in nonsprouting lineages (Wells, 1969
), although recent investigation has found mixed support for this diversification hypothesis (Bond and Midgley, 2003
). To what extent a changing environment might select for reduced generation time is unknown. Even during periods of rapid climate change, migration might buffer plants from experiencing severely changing selective pressures (Ackerly, 2003
).
This experiment is the first to examine intraspecific variation in resprouting behavior. Although no differences in overall growth rate were detected, the results generally support the findings of previous interspecific studies, in which sprouters exhibit greater carbohydrate storage, and suggest a trade-off between sexual and vegetative reproduction.
FOOTNOTES
1 The authors thank S. Davis (Pepperdine University, Malibu, California) and J. Keeley (U.S. Geological Survey, WERC, Sequoia-Kings Canyon Research Station, California) for unpublished observations, Radika Bhaskar and Katherine Preston for advice and assistance, and the numerous Stanford undergraduates who helped with the harvests. This work was in part supported by a grant from the Center for Evolutionary Studies (Stanford) and by NSF grant 0078301 to David Ackerly. 
2 Author for correspondence: Current address, U.S. Geological Survey, WERC, Sequoia-Kings Canyon Research Station, Three Rivers, CA 93271 USA; dschwilk{at}usgs.gov
; telephone: 559 565-3174; fax: 559 565-3177
LITERATURE CITED
Ackerly D. D 2003 Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences 164: S165-S184[CrossRef]
Bell D. T 2001 Ecological response syndromes in the flora of southwestern Western Australia: fire resprouters versus reseeders. Botanical Review 67: 417-440
Bell T. L F Ojeda 1999 Underground starch storage in Erica species of the cape floristic region: differences between seeders and resprouters. New Phytologist 144: 143-152[CrossRef][ISI]
Bell T. L J. S Pate 1996 Growth and fire response of selected Epacridaceae of southwestern Australia. Australian Journal of Botany 44: 509-526[CrossRef]
Bellingham P. J 2000 Resprouting as a life history strategy in woody plant communities. Oikos 89: 409-416[CrossRef][ISI]
Bond W. J J. J Midgley 2001 Ecology of sprouting in woody plants: the persistence niche. Trends in Ecology & Evolution 16: 45-51
Bond W. J J. J Midgley 2003 The evolutionary ecology of sprouting in woody plants. International Journal of Plant Sciences 164: S103-S114[CrossRef][ISI]
Bond W. J B. W van Wilgen 1996 Fire and plants. Population and community biology, vol. 14. Chapman and Hall, London, UK
Bowen B. J J. S Pate 1993 The significance of root starch in postfire shoot recovery of the resprouter Stirlingia latifolia R. Br. (Proteaceae). Annals of Botany 72: 7-16
Carpenter F. L H. F Recher 1979 Pollination, reproduction, and fire. American Naturalist 113: 871-879[CrossRef][ISI]
Charnov E W Shaffer 1973 Life history consequences of natural selection: Cole's result revisited. American Naturalist 117: 923-943[CrossRef]
da Silveira A. J F. F. F Teles J. W Stull 1978 Rapid technique for total nonstructural carbohydrate determination of plant tissue. Journal of Agricultural and Food Chemistry 26: 770-772[CrossRef]
Davis S K Kolb K Barton 1998 Ecophysiological processes and demographic patterns in the structuring of California chaparral. In P. W. Rundel, G. Montenegro Rizzardini, and F. M. Jaksic [eds.], Landscape disturbance and biodiversity in Mediterranean-type ecosystems. Ecological studies / Analysis and synthesis, vol. 136, 298–310. Springer, New York, New York, USA
Davis S. D F. W Ewers J. S Sperry K. A Portwood M. C Crocker G. C Adams 2002 Shoot dieback during prolonged drought in Ceanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure. American Journal of Botany 89: 820-828
Davis S. D F. W Ewers J Wood J. J Reeves K. J Kolb 1999 Differential susceptibility to xylem cavitation among three pairs of Ceanothus species in the transverse mountain ranges of southern California. Ecoscience 6: 180-186[ISI]
Enright N. J D Goldblum 1999 Demography of a non-sprouting and resprouting Hakea species (Proteaceae) in fire-prone eucalyptus woodlands of southeastern Australia in relation to stand age; drought and disease. Plant Ecology 144: 71-82
Field C. B C. P Lund N. R Chiariello B. E Mortimer 1997 CO2 effects on the water budget of grassland microcosm communities. Global Change Biology 3: 197-206
Frazer J S Davis 1988 Differential survival of chaparral seedlings during the first summer drought after wildfire. Oecologia 76: 215-221[CrossRef][ISI]
Hardig T. M P. S Soltis D. E Soltis 2000 Diversification of the North American shrub genus Ceanothus (Rhamnaceae): conflicting phylogenies from nuclear ribosomal DNA and chloroplast DNA. American Journal of Botany 87: 108-123
Hilbert D 1987 A model of life history strategies of chaparral shrubs in relation to fire frequency. In J. D. Tenhunen, F. M. Catarino, O. L. Lange, and W. C. Oechel [eds.], Plant responses to stress: functional analysis of Mediterranean ecosystems, 597–606. Springer-Verlag, Berlin, Germany
Jaks P 1984 The drought tolerance of Adenostoma fasciculatum and Ceanothus crassifolius seedlings and vegetation change in the San Gabriel chaparral. Master's thesis, San Diego State University, San Diego, California, USA
Keeley J. E 1977 Seed production, seed populations in soil, and seedling production after fire for two congeneric pairs of sprouting and non-sprouting chaparral shrubs. Ecology 58: 820-829[CrossRef][ISI]
Keeley J. E S. C Keeley 1977 Energy allocation patterns of a sprouting and a nonsprouting species of Arctostaphylos in the California chaparral. American Midland Naturalist 98: 1-10[CrossRef][ISI]
Keeley J. E P. H Zedler 1977 Reproduction of chaparral shrubs after fire: a comparison of sprouting and seeding strategies. American Midland Naturalist 99: 143-161
Kelly V. R V. T Parker 1990 Seed bank survival and dynamics in sprouting and nonsprouting Arctostaphylos species. American Midland Naturalist 124: 114-123[CrossRef][ISI]
Kummerow J G Montenegro D Krause 1981 Biomass, phenology and growth. In P. Miller [ed.], Resource use by chaparral and matorral, 69–96. Springer-Verlag, New York, New York, USA
Lamont B 1985 The comparative reproductive biology of three Leucospermum species (Proteaceae) in relation to fire responses and breeding system. Australian Journal of Botany 33: 139-145[CrossRef][ISI]
McMinn H. E 1939 An illustrated manual of California shrubs. University of California Press, Berkeley, California, USA
Meney K. A K. W Dixon J. S Pate 1997 Reproductive potential of obligate seeder and resprouter herbaceous perennial monocots (Restionaceae; Anarthriaceae; Ecdeiocoleaceae) from southwestern Western Australia. Australian Journal of Botany 45: 771-782[CrossRef]
Pate J. S R. H Froend B. J Bowen 1990 Seedling growth and storage characteristics of seeder and resprouter species of Mediterranean-type ecosystems of S.W. Australia. Annals of Botany 65: 585-601
Pate J. S K. A Meney K. W Dixon 1991 Contrasting growth and morphological characteristics of fire-sensitive (obligate seeder) and fire-resistant (resprouter) species of Restionaceae (S. Hemisphere restiads) from southwestern Western Australia. Australian Journal of Botany 39: 505-525[CrossRef]
Poole D S Roberts P Miller 1981 Water utilization. In P. Miller [ed.], Resource use by chaparral and matorral, 123–149. Springer-Verlag, New York, New York, USA
Pratt S. D A. S Konopka M. A Murry F. W Ewers S. D Davis 1997 Influence of soil moisture on the nodulation of post fire seedlings of Ceanothus growing in the Santa Monica Mountains of Southern California. Physiologia Plantarum 99: 673-679[CrossRef]
Schwilk D. W B Kerr 2002 Genetic niche-hiking: an alternative explanation for the evolution of flammability. Oikos 99: 431-442[CrossRef][ISI]
Thomas C. M S. D Davis 1989 Recovery patterns of three chaparral shrub species after wildfire. Oecologia 80: 309-320[CrossRef][ISI]
Thornton P S Running M White 1997 Generating surfaces of daily meteorological variables over large regions of complex terrain. Journal of Hydrology 190: 214-251[CrossRef][ISI]
Topp G J Davis A Annan 1980 Electromagnetic determination of soil water content: measurement in coaxial transmission lines. Water Resources Research 16: 574-582[ISI]
Warton D. I N. C Weber 2002 Common slope tests for bivariate errors-in-variables models. Biometrical Journal 44: 161-174[CrossRef][ISI]
Wells P. V 1969 The relation between mode of regeneration and extent of speciation in woody genera of the California chaparral. Evolution 23: 264-267[CrossRef][ISI]
Wiens D E. J King D. L Nickrent C. L Calvin N. L Vivrette 1989a Embryo and seed abortion in plants: reply. Nature 342: 626[CrossRef]
Wiens D D. L Nickrent C. I Davern C. L Calvin N. J Vivrette 1989b Developmental failure and loss of reproductive capacity in the rare paleoendemic shrub Dedeckera eurekensis. Nature 338: 65-67[CrossRef]
Williams J S Davis K Portwood 1997 Xylem embolism in seedlings and resprouts of Adenostoma fasciculatum after fire. Australian Journal of Botany 45: 291-300[CrossRef]
Zammit C M Westoby 1987 Seedling recruitment strategies in obligate-seeding and resprouting Banksia shrubs. Ecology 68: 1984-1992[CrossRef][ISI]
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