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Anatomy and Morphology |
2Unitat de Biologia Vegetal, Dept. de Ciències Ambientals, Universitat de Girona, Campus de Montilivi, 17071-Girona, Spain; 3Depto. de Biología Vegetal y Ecología, Universidad de Sevilla. Apdo. 1095, 41080-Sevilla, Spain
Received for publication October 18, 2001. Accepted for publication March 19, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Cape Floristic Region • Erica • Ericaceae • fynbos • lignotuber • post-fire regeneration • root : shoot ratio • starch storage tissue
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Keeley, 1986
; Cowling, 1987
; but see Mesléard and Lepart, 1989
; López-Soria and Castell, 1992
; and Ojeda, 2001
for a critical view from the Mediterranean Basin). Generally, woody species are grouped into two categories according to their post-fire response: seeders and resprouters (Bond and van Wilgen, 1996
). Seeder plants are killed by fire, with stands being reestablished by a massive seedling recruitment from a preexisting, soil- or canopy-stored seed bank. Resprouter plants, by contrast, survive the complete removal of all the aerial parts by fire, and recover relatively quickly by growth of dormant buds protected from the action of fire, either by thick bark or by location near the soil surface, irrespective of their effectiveness on post-fire seedling emergence. Although both seeder and resprouter post-fire responses imply resilience to recurrent wildfires at the population level, their effects in the dynamics of populations are altogether different. Each fire means a complete generation turnover for seeder populations, being nonoverlapping generations (assuming that seed germination is induced by fire, e.g., see Keeley and Bond, 1997
). Besides, seeder populations will be prone to dramatic size fluctuations (i.e., bottlenecks) between fires, whereas resprouter populations are somewhat buffered from such fluctuations because of the ability of resprouter adult individuals to survive fire. These differences in the population dynamics have crucial consequences in the long-term diversification patterns of seeder and resprouter lineages (Wells, 1969
; Ojeda, 1998
).
Post-fire sprouting of dormant buds is boosted by stored nutrient and carbohydrate reserves. The major critical carbohydrate reserve in resprouter plants is starch (Miyanishi and Kellman, 1986;
Pate et al., 1990
; Verdaguer et al., 2001
). Several authors have claimed the role of swollen underground structures such as root-crowns, burls, or lignotubers as specialized organs for starch storage (e.g., Bamber and Mullette, 1978
; Canadell and López-Soria, 1998
) and a placement for dormant buds (James, 1984
; Molinas and Verdaguer, 1993a
, b
). However, other authors argue that these structures are no more efficient than woody roots as tissues for starch storage (e.g., Cruz and Moreno, 2001
) and that the selective advantage of developing a swollen underground structure is mainly related to the large amount of concealed buds found on its surface in a protected position close to the ground (Carrodus and Blake, 1970
).
Starch is mainly stored within xylem parenchyma ray tissue of underground organs (Loescher, McCamant, and Keller, 1990
; Pate et al., 1990
; Bell, Pate, and Dixon, 1996
; Bell and Ojeda, 1999
). This type of storage tissue can be considered to be expensive in terms of resource allocation as ray parenchyma cells of wood are living and non-photosynthetic (Salisbury and Ross, 1992
; Bowes, 1996
) and require a high metabolic demand to be both created and maintained. In addition, the synthesis of starch to fill such cells detracts from the pool of carbon that could otherwise be invested in photosynthetic tissue. Therefore, allocation to underground starch storage would imply a physiological trade-off for the plant in terms of allocation to aboveground growth of photosynthetic parts (Bloom, Chapin, and Mooney, 1985
; Iwasa and Kubo, 1997
; Sakai, Sakai, and Akiyama, 1997
).
The South African Cape Floristic Region includes one of the five mediterranean regions of the world (Cody and Mooney, 1978
). Despite its relatively small size (90 000 km2), this region is one of the world's richest areas in plant diversity (Goldblatt, 1997
). Most taxa show a pattern of high species concentration and endemism in fynbos, the most characteristic vegetation-type in this region. Poor soils, mediterranean or semi-mediterranean climate, and the recurrence of summer wildfires constitute the main selective regime of fynbos (Cowling, 1992
). The genus Erica, with approximately 600 species, represents a paradigm amongst the highly speciated taxa of the fynbos (Goldblatt, 1997
).
About 90% of Cape Erica species are seeders (Oliver, 1991
; Ojeda, 1998
). Only 6% are resprouters, capable of surviving fire and resprouting from developed underground lignotubers. The remaining 4% of species, termed "mixed" species by Ojeda (1998)
, includes distinct resprouter and seeder individuals, generally in well-separated populations. In a recent study, Bell and Ojeda (1999)
found that adult resprouter individuals of three "mixed" species had consistently higher percentages of parenchymatic ray tissue and accumulated more starch in roots than their seeder counterparts. Are these phenotypic differences in allocation to root storage fixed attributes, happening from early seedling stages or are they a consequence of environmental differences experienced during development of the plant?
In this paper, we present the results of a comparative analysis of (1) the pattern of starch storage, (2) the proportion of parenchymatic ray tissue in upper regions of the root system, and (3) the root-to-shoot allocation pattern between seedlings of seeder and resprouter forms of two "mixed" Cape Erica species: E. coccinea L. and E. calycina L., raised under controlled glasshouse conditions. This common garden approach is aimed to determine if the source of phenotypic variation in allocation to root storage in Erica species is genetically determined or, by contrast, may be better viewed as an example of environmentally driven phenotypic plasticity (see Futuyma, 1998
). Moreover, this study will reveal important information about the ontogenetic formation of the lignotuber in the resprouter forms of these two species. Although caution must be taken, the intraspecific approach of this seeder versus resprouter comparison implemented in two different species allows us to make inferences about patterns of root starch storage in seeder and resprouter Erica lineages at the seedling stage. The implications of the results of this study are of paramount importance to developing a better understanding of the biogeography and the evolutionary history of the genus Erica in the Cape Floristic Region (Ojeda, 1998
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Trays were housed under greenhouse conditions at the University of Sevilla (Seville, Spain) and were kept moist by controlled irrigation. Germination started about 1 mo after sowing, but was not synchronous, since seeds were not smoke-treated (see Brown, Kotze, and Botha, 1993
). Harvesting of seedlings took place in January 2000, 9 mo after sowing, while some seedlings were still germinating. Harvested seedlings were classified into two age classes: young (1.0 cm < shoot length < 3.0 cm) and old (3.0 cm < shoot length < 9.0 cm) seedlings, using shoot length as a approximate surrogate of seedling developmental stage.
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). Transverse sections 3–5 µm thick were obtained by using a rotatory microtome Autocut 1150 (Reichert-Jung, Wien, Austria) and mounted on glass slides. Sections were stained with thionin or 2% iodine solution (I2KI) for detection of starch granules. Samples were viewed with an Olympus-Vanoxlight microscope (Olympus Optical, London, UK). For anatomical purposes, ray parenchyma cells, inter-ray parenchyma cells, and wide vessel elements of root material were readily distinguishable even in young seedlings. Ray parenchyma cells were those living cells disposed radially, regardless of whether they contained starch or not (Figs. 1–5). Xylem parenchyma rays were classified as being uniseriate when they remained one cell wide from close to the center of the root to the outermost region of the root to just below the phloem. Rays were classified as being multiseriate when they were two or more cells wide at the outermost region of the root. Inter-ray parenchyma cells were those lying between xylem rays (1) having very wide lumina with or without a secondary wall, (2) having no secondary cell wall, and/or (3) filled with starch grains (see Figs. 1, 2, 4). Xylem vessels were considered to be those cells more than 8 µm in diameter and never filled with starch (see Figs. 3–5). Finally, cells with small lumens and secondary cell walls that were never filled with starch constituted the remainder of vascular tissue, narrow vessel elements, tracheids and fibers, all of which were often difficult to distinguish from each other owing to the presence of transitional forms.
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Root-to-shoot allocation
Aboveground (shoot) dry biomass and root thickness (cross-section diameter) at 1 cm below the cotyledonary node were recorded in young and old seedlings. We established allometric relationships between these two variables in order to explore possible differences in the root-to-shoot allocation pattern between seeder and resprouter forms (see below).We used root thickness as an indicator of root dry biomass as it was not possible to harvest seedlings for anatomical purposes and not damage their root system.
Statistical analyses
We tested the differences between regeneration forms in (1) the relative amount of root starch, (2) the proportion of ray parenchyma root tissue, and (3) the proportion of starch-filled ray parenchyma root tissue, for each species. Because the response variable, in the three instances, was measured repeatedly in a number of image fields from each individual plant root cross-section (see above), we used the following model to describe the data: Xijk = µ + 
i + ßj(i) + 
ijk. This model corresponds to a hierarchically nested ANOVA design. Xijk is any replicate image field quantitative determination (k) of the response variable in any of the eight replicate seedling cross-sections (j) in any of the two regeneration forms (i); the term µ denotes the population grand mean, i.e., the mean value of all image field observations in all the individual seedlings sampled; i is the ith level of the main effect (regeneration, fixed factor); the ßj(i) term stands for the mean of k image field observations in the jth seedling cross-section (seedling, random factor) nested in the ith regeneration form; finally, the ijk term is the random error, representing the individual variability from one image field observation to another within a particular seedling cross-section. It should be made clear that the i x j individual seedling cross-sections, not the i x j x k image fields, are the experimental units in this nested design, thus overcoming pseudoreplication (see Underwood, 1997
). Probability levels of P < 0.05 were regarded as significant throughout the analyses.
We also estimated the relative contribution of individual factors to the response variables in the ANOVAs by determining their magnitude effects (
2) through calculating their variance components (Graham and Edwards, 2001
). Unfortunately, methods detailed by Graham and Edwards (see also Underwood, 1997
) only consider balanced designs, whereas our data were strongly unbalanced. To overcome this difficulty, we obtained the average sample size (n0) within each ij level using the computations described in Sokal and Rohlf (1995)
and replaced n by n0 in Graham and Edwards' (2001)
formulae for nested ANOVAs.
Size (root diameter) of the seedlings used in this study was not constant nor homogeneous across species; whereas seeder and resprouter E. calycina seedlings did not show significant differences [seeder (S): 0.4 ± 0.1 mm (mean ± SD); resprouter (R): 0.6 ± 0.2 mm; t = –1.87, df = 14, P = 0.08), seeder E. coccinea seedlings were larger than resprouters and had slightly but significantly thicker root diameters than resprouter ones (S: 0.5 ± 0.1 mm; R: 0.3 ± 0.1 mm; t = 3.46, df = 14, P < 0.01). However, considering root diameter as a covariate did not qualitatively change the results, so it was not included in the ANOVAs. Over-parameterized model estimation and type III sums of squares were used to fit the data, using the STATISTICA visual GLM module (StatSoft, 1999
). Data, given in percentages, were arcsine-transformed prior to analyses to deal with heteroscedasticity and nonnormality (Sokal and Rohlf, 1995
).
The relationship between shoot dry biomass and root thickness was determined for each species and regeneration form using simple linear regression analysis. We tested the existence of different regression slopes between seeder and resprouter forms, for each species, by means of analysis of covariance (Underwood, 1997
). This analysis allowed us to ascertain whether seeder and resprouter seedlings differed in their root to shoot patterns of biomass allocation.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Young resprouter seedlings of both species of Erica showed a higher relative amount of starch in roots than their seeder counterparts (Table 2; Fig. 6). This starch was mostly stored in parenchymatic xylem rays (Figs. 2, 4), although some inter-ray parenchyma cells were also found to contain starch, particularly in resprouter seedlings of E. coccinea (Fig. 4).
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2 < 15%) to the total sums of squares of these two response variables. Most of the variation of these two variables, as well as the variation in the proportion of ray parenchyma tissue in upper roots, was explained by the regeneration effect (see Tables 2–4). Transverse sections from old seedlings (i.e., 3.0 cm < shoot length < 9.0 cm) showed contrasting patterns of xylem parenchymatic rays in relation to width and starch distribution between seeder and resprouter regeneration forms of both species (Figs. 9–12). Old seedlings of resprouter E. calycina consistently had both broad (multiseriate) and thin (uniseriate) rays with most of the cells in this tissue type having large amounts of starch grains. This seedling type also had some starch-filled inter-ray parenchyma cells (Fig. 9). Comparable seedlings of seeder E. calycina did not possess any broad parenchyma rays and most rays were uniseriate or a maximum of two cells wide. Cells of rays and inter-ray parenchyma did not generally contain starch (Fig. 10).
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Root-to-shoot allocation
Differences between seeder and resprouter seedlings in the diameters of the upper portions of the root system and the cotyledonary node region were readily distinguishable in old seedlings of both species (Fig. 13). We also observed greater numbers of buds in the cotyledonary region of resprouter seedlings than in seeder seedlings, particularly for E. coccinea (Fig. 13). Strong positive correlations were detected between the diameters of the upper portions of the root system and the dry mass of the shoots for young and older seedlings of both species and regeneration forms (Table 5). Regression slopes in seeder seedlings were significantly steeper than those of resprouter seedlings in both E. calycina and E. coccinea (Table 5), with such differences being more marked in E. calycina (Fig. 14).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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found that, contrary to expectation, seedlings of certain woody species that as adults had higher allocation to root biomass than others showed lower root allocations when grown individually in enriched conditions in the greenhouse. They concluded that root-to-shoot allocation patterns should be viewed as plastic responses to environmental conditions rather than fixed species attributes. In a recent study, Bell and Ojeda (1999)
found that starch and storage tissue in roots in adult plants of resprouter lineages of Cape Erica species was consistently higher than in seeders. Could this within-species allocation to starch storage in roots be used as an example of environmentally driven phenotypic plasticity? The comparative study presented here has revealed that differences between seeders and resprouters in allocation to underground (root) starch storage can be detected in early seedling stages in two "mixed" Erica species, E. calycina and E. coccinea, when raised under common garden conditions. Significant differences in the relative amount of xylem ray tissue (i.e., proportion of ray parenchyma cells) present in differing regeneration forms was detected in E. calycina but not in E. coccinea (see Table 3). The small sample size (eight individuals per species and regeneration form) as well as the fact that sampled young seedlings of the resprouter form of E. coccinea were slightly smaller and had significantly thinner root diameters than sampled seeder ones (see MATERIALS AND METHODS) might account for the lack of significant difference in this species. If old seedlings had been also included in the analysis we would have undoubtedly recorded significant differences, since wider parenchyma rays were obvious in these individuals (see Figs. 9–12). Notwithstanding, it must be borne in mind that "old seedlings" were never older than 9 mo, i.e., still certainly young.
Despite rendering significant, the seedling effect contributed very little to the variation in the relative amount of root starch and the percentage of starch-filled ray parenchyma cells compared to the regeneration effect. We can thus infer that the regeneration form consistently accounts for most of the within-species variability of allocation to underground (root) starch storage in Erica seedlings. Pate et al. (1990)
described a pattern of differential allocation to root starch in seeder and resprouter pairs of co-generic shrub species at the seedling (2–4 yr old) stage. However, our study must not be seen merely as a further contribution to reinforce this pattern. We emphasize that the seeder–resprouter comparisons are within species and implemented in two different Erica species, which enables us to factor out possible "phylogenetic constraints" (Ackerly and Donoghue, 1995
; Ricklefs, 1996
; Silvertown and Dodd, 1996
) and allows us to make generalizations to the genus Erica in the Cape region, although caution must be taken. Thus, the contrasted allocation to root starch storage between seeder and resprouter Erica lineages, previously detected in adult plants by Bell and Ojeda (1999)
, occurs from the earliest seedling stages. Moreover, the fact that seedlings were grown under controlled glasshouse conditions allows us to infer that it is a genetically determined and fixed attribute in this genus rather than an example of environmentally driven phenotypic plasticity.
The swelling of the upper root region and the observation of plentiful buds in the cotyledonary region of resprouter seedlings, presumably confering high sprouting capacity, suggest that not only are there differences in starch storage capacity and storage realization in roots, but that there is also the facility to develop a lignotuber early on in seedling development. Further studies are needed to confirm the presence of dormant buds in the cotyledonary region of resprouter and seeder forms and to follow the development of this region in later stages of seedling growth.
Higher allocation to underground starch storage and specialized storage tissue, which is expensive to create and maintain (Bloom, Chapin, and Mooney, 1985
; Chapin, Schulze, and Mooney, 1990
; Sakai, Sakai, and Akiyama, 1997
), would imply a reduced aboveground biomass accumulation in resprouters (Pate et al., 1990
; Bell and Pate, 1996
). The different regression slopes relating root thickness to aboveground dry biomass between seeder and resprouter forms of both Erica species could be interpreted as a reflection of this root-to-shoot allocation trade-off from the earliest stages of seedling development.
The retarded aboveground growth of seedlings of resprouter lineages compared to those of seeders may render resprouter seedlings less able to withstand a seasonal (summer) soil moisture stress (see Taylor, 1989
). Although it remains to be tested, this presumably higher sensitivity of resprouter Erica seedlings to summer drought in the first stages of establishment had been previously assumed by Ojeda (1998)
in order to explain the selection of Erica seeder lineages, more prone to speciation (Wells, 1969
), in the mild mediterranean southwestern Cape region.
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FOOTNOTES |
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4 Author for reprint requests (current address: Depto. de Biología, CASEM, Universidad de Cádiz. Campus Río San Pedro, 11510- Puerto Real, Spain; fernando.ojeda{at}uca.es
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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