| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Ecology |
Division of Biology, Kansas State University, Manhattan, Kansas 66506 USA
Received for publication June 5, 2003. Accepted for publication October 30, 2003.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: fire • rhizomes • seed bank • tallgrass prairie
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
) plays a fundamental role in local plant population structure and dynamics.
Understanding the relative contributions of sexual and vegetative reproduction is of great importance as they can strongly influence genetic diversity, spatial pattern, and dynamics of plant populations. For example, a reserve of dormant seeds in the soil can stabilize plant population dynamics and may influence their sensitivity or resilience to environmental change. The seed bank can also provide a reserve of genetic variability when long-lived dormant seeds act as a memory of past selection or as a source of new genetic variation through accumulating mutations (Levin, 1990
). The relative abundance of species in belowground bud or seed populations may differ significantly from those of the aboveground community, thereby influencing the structure and dynamics of plant communities and their responses to disturbance. The belowground bud bank has the potential to influence patterns of net primary production in some ecosystems, such as grasslands, where "meristem limitation" may constrain primary production and its inherent temporal variability (Knapp and Smith, 2001
). The general ecological and evolutionary consequences of seed banks have been well studied (see reviews in Fenner, 1985
; Baskin and Baskin, 1998
). However, despite the importance of belowground bud banks in many systems, few empirical or theoretical studies have examined their patterns, dynamics, or consequences (Busso et al., 1989
; Tuomi et al., 1994
; Hendrickson and Briske, 1997
).
In North American tallgrass prairie and other perennial-dominated grasslands, the seasonal regeneration of aboveground shoots occurs principally via tillering or vegetative reproduction by rhizomes. The meristem populations of the rhizome system are thus of much greater importance to local population dynamics than are seed banks (Hartnett and Keeler, 1995
; Hartnett and Fay, 1998
). Although viable seed populations ranging from a few hundred to >6000 seeds/m2 may occur in tallgrass prairie (Weaver and Mueller, 1942
; Rabinowitz, 1981
), successful seedling establishment is a rare event, by some estimates contributing <1% of total aboveground stems (Christiansen and Landers, 1966
; Thompson and Grime, 1979
; Glenn-Lewin et al., 1990
; Benson, 2001
; Rogers and Hartnett, 2001
). Rhizome-derived tillers and ramets have a greater ability than seedlings to emerge through the low light conditions of accumulated unburned detritus and have greater competitive ability once they emerge, presumably because of their developed root system, stored food reserves, and the potential for physiological integration among ramets (Hartnett and Keeler, 1995
). Indeed, new inputs to the genetic composition of prairie plant populations from seed may be rare enough to restrict the ability of grassland populations to adapt to environmental change (Hedrick and Miller, 1992
; but see also Whitham and Slobodchikoff, 1981
; Ellstrand and Roose, 1987
).
In tallgrass prairie and other grasslands, fire frequency strongly influences plant species composition and diversity and has the potential to affect the belowground bud bank. Frequent fire, especially in the spring season, and the concomitant regular removal of the litter layer favors the dominant C4 warm-season grasses and leads to increased tiller density, high dominance, and low species diversity. Infrequent fire increases the abundance of C3 graminoids (grasses and sedges) and perennial dicot herbs (forbs), resulting in higher evenness and plant species diversity (Aldous, 1934
; Kucera and Koelling, 1964
; Collins and Wallace, 1990
). However, other factors, such as grazing by large herbivores, may reduce the abundance of the dominant grasses, resulting in competitive release of the subordinate grasses and forbs, which offsets the effects of frequent fire and enhances plant species diversity (Hartnett and Fay, 1998
). The underlying demographic mechanisms driving these complex community responses are poorly known, and the few studies that have examined prairie seed banks indicate that the composition and densities of dormant seeds in the soil are poor predictors of aboveground plant community responses (Rabinowitz and Rapp, 1980
; Abrams, 1988
). In these grasslands, the interacting effects of fire, grazing, climate, and management practices on belowground meristem populations are likely to be a primary driver of patterns of aboveground community structure and productivity.
The primary objective of this study was to quantify the size and spatial and temporal variability of the grass and forb rhizome bud bank of tallgrass prairie and to determine whether the relative abundance of grass and forb meristem populations belowground was a good predictor of aboveground plant community structure. In addition, rhizome bud densities and composition were quantified on annually burned and infrequently burned prairie to determine the potential effect of large-scale disturbances, such as fire, on the population of belowground vegetative meristems and on the relative contributions of grasses and forbs to the soil bud bank. These results were compared to data from a previous study that examined seed bank density and composition on the same site (Abrams, 1988
) to compare fire effects on these two belowground populations. Finally, belowground meristem densities were compared to densities of established stems to provide insight into the extent to which meristem limitation may regulate plant population abundance and productivity in tallgrass prairie.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
KPBS is divided into 60 watershed units (average size, 60 ha), and prescribed burn treatments are applied and replicated at the watershed scale. Five watersheds were sampled in this investigation. At the time of the study, three watersheds, 1C, 1D, and SpB, had been burned annually in the spring since 1972, 1978, and 1996, respectively. The other two watersheds, 20B and 20C, were on a planned 20-yr fire cycle. They were last burned by wildfire in the spring of 1991.
In November of 1997 and 1998, rhizome bud banks were sampled by taking soil cores, each 10.5 cm in diameter and 15 cm deep, from random locations in the lowlands of watersheds 1C, 1D, 20B, and 20C. Ten replicate cores were taken from random locations within each site. Preliminary core sampling and a concurrent study at KPBS (Elder, 2001
) revealed that the mean depth of grass and forb rhizomes in upland and lowland sites was 3.2 ± 2.1 cm, and rhizomes and perennating buds were rarely found at depths greater than 12 cm (although the roots of some taprooted forbs extend much deeper). Stems on the surface of each core were counted to estimate aboveground plant stem density. The soil was then removed, and living rhizome meristems were counted and identified as grass or forb. Rhizome bud morphology of grasses and forbs are distinct and easily identifiable. For both forbs and grasses, the numbers of living rhizomes and rhizome buds were summed to estimate the total number of belowground meristems (potential new ramets) per core. Random lowland core samples were collected in the same manner from watersheds 1D, SPB, 20B, and 20C at three times during the 2001 growing season (early June, late July, and late September) to explore temporal variation in rhizome bud bank densities across the growing season and among years. Watershed 1C was not sampled in 2001 because it was converted to a different burn regimen and had not been burned that spring.
Because of large variation and non-normal distribution of meristem densities per core, the bud bank data were rank transformed prior to analysis. The ranked data were analyzed using a 2 x 2 factorial ANOVA (Conover and Iman, 1981
). The factors examined were burn treatment and year. Bud bank densities were calculated from the core sample data. For comparison, soil seed bank data from a previous study conducted on KPBS (Abrams, 1988
) were also recomputed to estimate total densities of grass and forb seeds in annually burned and infrequently burned prairie.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
Data from a previous study on seed bank densities on the annually burned and infrequently burned sites at KPBS (Abrams, 1988
) were recalculated and expressed on a seeds per square meter basis. Note that the two sets of data were derived from different sampling sites at KPBS in different years and thus are not directly comparable. However, both studies were conducted using the same replicated watershed-level fire frequency treatments at KPBS and are useful for a general comparison of trends in the seed bank and bud bank populations. Notably, seed and bud banks respond differently to fire. Abrams' (1988)
estimates of the total viable seed bank in annually burned KPBS uplands are similar in magnitude to that of the total rhizome bud bank in annually burned prairie (1453 seeds/m2 vs. 1366 buds/m2), whereas in unburned prairie the estimated total seed bank population is more than four times that of the belowground meristem population (2892 seeds/m2 vs. 693 buds/m2). In contrast to the bud bank populations, as well as aboveground plant populations, grass seed densities were lower in annually burned than in unburned sites (788 seeds/m2 vs. 2267 seeds/m2), whereas forb viable seed densities did not differ greatly between burned and unburned prairie (677 seeds/m2 vs. 625 seeds/m2). Thus, primarily as a result of the grass response to fire, frequent burning significantly reduced total soil seed bank densities but increased belowground bud bank densities in tallgrass prairie.
The coefficient of variation (CV) in bud densities among core samples was calculated in order to compare spatial variability among plant groups and burn treatments (Table 1). Spatial variability in belowground meristem populations was higher, on average, in the annually burned watersheds. This was primarily due to the high spatial variability of forb rhizome bud bank populations, which was 2–3 times greater than that of grass rhizome buds or the total bud bank population, reflecting the patchiness of forb distribution, particularly in annually burned prairie.
|
). Thus, it was assumed that all of the 1997 stems had senesced and disappeared by the autumn of 1998 and that the contribution of seedlings to the established aboveground stem population was negligible. This comparison was used as an index of the degree to which belowground meristem populations may limit aboveground population densities. Mean rhizome bud and ramet densities and the ratio of buds : stems (meristem limitation index, MLI) are shown in Table 2. An MLI of 1.3 : 1 in annually burned prairie indicates that approximately 75% of the rhizome buds present in 1997 produced established stems in 1998. By contrast, in infrequently burned watersheds, the density of established stems in 1998 was nearly 1.5 times greater than the number of viable buds present the previous autumn (MLI = 0.7 : 1).
|
70% grass, 30% forb). Total rhizome bud population densities were similar across the three years sampled, indicating the presence of stable populations of belowground meristems that are potentially available for recruitment each year. In addition, fire frequency had similar effects on bud bank populations in all three years in that frequent fire decreased forb rhizome bud densities and increased grass and total bud bank densities relative to unburned sites.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
) and the principal mechanism of recolonization of small-scale animal-generated soil disturbances (Rogers and Hartnett, 2001
). Although reported densities of seed bank populations were of comparable size to our bud bank estimates, successful establishment from seed is rare, and thus seeds make a negligible contribution to local population maintenance. However, even rare additions of new genets from seed or accumulating mutations within the bud bank may be sufficient to maintain substantial levels of genetic variability in these clonal plant populations (e.g., Soane and Watkinson, 1979
; Whitham and Slobodchikoff, 1981
; Ellstrand and Roose, 1987
).
In this study, the relative densities of forb and grass rhizome buds generally reflected the aboveground patterns in species composition in annually burned and unburned prairie. Higher relative densities of belowground forb meristems in infrequently burned prairie soils corresponded to the relatively greater abundance of forbs in the aboveground plant community commonly found in these sites, and higher grass rhizome bud population densities in annually burned prairie reflected the greater relative abundance of grass tillers in these sites. However, examination of the seed bank data from the previous study at this site showed that the relative abundance of grass and forb viable seeds were opposite those of the rhizome bud populations and opposite those typically found in aboveground plant assemblages in annually and infrequently burned prairie (Abrams, 1988
). The fact that the grass : forb meristem ratio within the bud bank closely reflected patterns aboveground, whereas the seed bank composition did not, further strengthens the claim that aboveground plant community dynamics are driven strongly by patterns of vegetative reproduction and rhizome bud populations, rather than by reproduction via seed and seed bank dynamics.
Our results indicate that fire in tallgrass prairie strongly influences the production of belowground meristems and rhizome bud bank population size, contributing significantly to overall vegetation responses to fire. Total rhizome bud density increased with more frequent burning, and this increase was driven primarily by augmentation of the belowground grass bud population. Forb rhizome bud bank populations were much smaller and had the opposite response, increasing in density with a reduction in fire frequency. However, interannual variability was high. Spatial variability was higher, in general, in sites that were burned annually, and variability in forb bud densities was higher than that of grass bud densities. The strikingly higher spatial variability of forb rhizome buds on burned sites compared to unburned sites likely reflects the scarcity and relative patchiness of forbs in the aboveground perennial grass matrix of annually burned sites.
If belowground bud bank populations are indeed driving aboveground plant community composition in tallgrass prairie, aboveground population densities (and therefore aboveground net primary productivity) may be meristem limited. In annually burned prairie, the density of rhizome buds in the soil at the onset of the growing season significantly exceeded the density of ramets aboveground, suggesting that aboveground populations are not meristem limited when fire occurs frequently. However, it is possible that not all buds break dormancy in any given year, such that limited numbers of "active" rhizome buds may, in fact, regulate aboveground stem densities. Previous studies have shown that clonal growth patterns in tallgrass prairie grasses can be strongly regulated by competition (e.g., Hartnett, 1993
), and it is likely that competition for light, nutrients, or water, rather than meristem limitation, results in density-dependent ramet or tiller emergence and/or mortality rates, which in turn limit stem density. Despite the potential for strong competition to limit the growth and survivorship of newly emerging ramets, the estimated success rate of rhizome buds was orders of magnitude higher than rates of seed germination and establishment reported for several tallgrass prairie grasses and forbs (Christiansen and Landers, 1966
; Benson, 2001
).
In infrequently burned sites, the greater abundance of ramets than belowground meristems was unexpected and suggests that low fire frequencies result in a much greater potential for meristem limitation in tallgrass prairie. A relatively smaller reserve of available belowground rhizome buds may be important in explaining the lower stem densities and lower annual net primary production of infrequently burned prairie when compared to prairie that has been annually burned (Knapp et al., 1998
). However, several possible mechanisms and factors could partially explain an aboveground ramet density that exceeds the density of belowground vegetative meristems. Some stems present in 1997 on the unburned prairie, though senescent, may have remained erect through the dormant season, leading to their being counted with 1998 stems. This could have slightly inflated estimates of 1998 stem density in unburned populations only, as all previous year's stems are consumed by fire in the annually burned site. However, such potential for errors in distinguishing current from previous year's ramets is small and cannot account for the large difference in bud : stem ratios between treatments observed in this study.
It is also unlikely that stem densities exceeding rhizome bud densities in unburned sites can be explained by seedling recruits, given the extreme rarity of successful seedling establishment of perennial grasses and forbs in tallgrass prairie (Benson, 2001
). The interference of detritus, competitive suppression by established plants, and low light and soil temperature conditions on unburned prairie (Knapp et al., 1998
) greatly constrain seedling success. We hypothesize that these environmental conditions on unburned prairie may also lead to low natality rates in rhizome bud populations, which may be the primary mechanism resulting in greater meristem limitation in the absence of fire. The higher bud densities in annually burned prairie and a recent study demonstrating that rhizome bud populations are well insulated from direct damage from fire (Elder, 2001
) both suggest that a difference in bud population natality rate, rather than mortality rate, is the principal mechanism accounting for fire effects on aboveground plant population dynamics.
The production of an early spring cohort of additional new rhizome buds may result in a higher number of meristems available than estimated from our summer and autumn censuses. Indeed, the patterns of bud densities observed over the 2001 growing season suggest that bud bank densities may reach their maximum in early spring. Although our study provides good estimates of the size and spatio-temporal variability of bud banks in tallgrass prairie and addresses the effects of fire, a more detailed study of the demography of belowground bud populations (both birth and loss rates) over an annual growth cycle will be necessary to assess accurately the maximum densities of buds available for shoot production and to quantify accurately the degree of meristem limitation.
The data presented here indicate that belowground meristem populations play an important role in aboveground vegetation dynamics in tallgrass prairie and suggest that patterns of variability in plant abundance and productivity aboveground associated with natural disturbances (fire and grazing), climatic variability, or other factors may be mediated through effects on soil bud bank populations. Particularly, frequent fire increases grass rhizome density and decreases forb rhizome density relative to infrequently burned prairie. The bud bank closely reflects changes in aboveground species composition, whereas the seed bank does not. Aboveground stem densities may experience meristem limitation, either through a limited number of "active" rhizomes on burned prairie or a limiting total number of rhizomes on infrequently burned sites. However, season-long data suggest the existence of a late-emerging rhizome cohort that could account for greater stem density than bud bank density on unburned prairie. Meristem limitation may explain patterns of variability in productivity among different grasslands, and the incorporation of belowground bud bank dynamics into structured matrix models could improve our capacity to predict long-term population trends and responses to environmental change in these ecosystems. Our continued study of the demography of grassland plants and plant parts is addressing these questions, perhaps leading to greater insights into the role of bud banks in the changing composition and dynamics of grasslands.
|
FOOTNOTES |
|---|
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Aldous A. E. 1934 Effect of burning on Kansas bluestem pastures. Kansas Agricultural Experiment Station Technical Bulletin 38: 1-65
Baskin C. C. J. M. Baskin 1998 Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego, California, USA
Benson E. J. 2001 Effects of fire on tallgrass prairie plant population dynamics. M.S. thesis, Kansas State University, Manhattan, Kansas, USA
Busso C. A. R. J. Mueller J. H. Richards 1989 Effects of drought and defoliation on bud viability in two caespitose grasses. Annals of Botany 63: 477-485
Christiansen P. A. R. Q. Landers 1966 Notes on prairie species in Iowa. I. Germination and establishment of several species. Transactions of the Iowa Academy of Science 73: 51-59
Collins S. L. L. L. Wallace 1990 Fire in North American tallgrass prairies. University of Oklahoma Press, Norman, Oklahoma, USA
Conover W. J. R. L. Iman 1981 Rank transformations as a bridge between parametric and non-parametric statistics. American Statistician 35: 124-129[CrossRef][ISI]
Elder B. D. 2001 The effects of fire on the life history traits of tallgrass prairie forbs. Ph.D. dissertation, Kansas State University, Manhattan, Kansas, USA
Ellstrand N. C. M. L. Roose 1987 Patterns of genotypic diversity in clonal plant species. American Journal of Botany 74: 123-131[CrossRef][ISI]
Fenner M. 1985 Seed ecology. Chapman and Hall, New York, New York, USA
Glenn-Lewin D. C. L. A. Johnson T. W. Jurik A. Akey M. Leoschke T. Rosberg 1990 Fire in central North American grasslands: vegetative reproduction, seed germination, and seedling establishment. In S. L. Collins and L. L. Wallace [eds.], Fire in North American tallgrass prairies, 28–45. University of Oklahoma Press, Norman, Oklahoma, USA
Harper J. L. 1977 Population biology of plants. Academic Press, New York, New York, USA
Hartnett D. C. 1993 Regulation of clonal growth and dynamics of Panicum virgatum in tallgrass prairie: effects of neighbor removal and nutrient addition. American Journal of Botany 80: 1114-1120[CrossRef][ISI]
Hartnett D. C. P. A. Fay 1998 Plant populations: patterns and processes. In A. K. Knapp, J. M. Briggs, D. C. Hartnett, and S. L. Collins [eds.], Grassland dynamics: long-term ecological research in tallgrass prairie, 81–100. Oxford University Press, New York, New York, USA
Hartnett D. C. K. H. Keeler 1995 Population processes. In A. Joern and K. H. Keeler [eds.], The changing prairie: North American grasslands, 82–99. Oxford University Press, New York, New York, USA
Hedrick P. W. P. S. Miller 1992 Conservation genetics: techniques and fundamentals. Ecological Applications 2: 30-46
Hendrickson J. R. D. D. Briske 1997 Axillary bud banks of two semiarid perennial grasses: occurrence, longevity, and contribution to population persistence. Oecologia 110: 584-591[CrossRef][ISI]
Knapp A. K. J. M. Briggs J. M. Blair C. L. Turner 1998 Patterns and controls of aboveground net primary production in tallgrass prairie. In A. K. Knapp, J. M. Briggs, D. C. Hartnett, and S. L. Collins [eds.], Grassland dynamics: long-term ecological research in tallgrass prairie, 193–221. Oxford University Press, New York, New York, USA
Knapp A. K. M. D. Smith 2001 Variation among biomes in temporal dynamics of aboveground primary production. Science 291: 481-484
Kucera C. L. M. Koelling 1964 The influence of fire on composition of central Missouri prairie. American Midland Naturalist 72: 142-147[CrossRef]
Levin D. A. 1990 The seed bank as a source of genetic novelty in plants. American Naturalist 135: 563-572[CrossRef][ISI]
Rabinowitz D. 1981 Buried viable seeds in a North American tallgrass prairie: the resemblance of their abundance and composition to dispersing seeds. Oikos 36: 191-195[CrossRef][ISI]
Rabinowitz D. J. K. Rapp 1980 Seed rain in a North American tall grass prairie. Journal of Applied Ecology 17: 793-802[CrossRef][ISI]
Rogers W. E. D. C. Hartnett 2001 Temporal vegetation dynamics and recolonization mechanisms on different-sized soil disturbances in tallgrass prairie. American Journal of Botany 88: 1634-1642
Soane I. D. A. R. Watkinson 1979 Clonal variation in populations of Ranunculus repens. New Phytologist 82: 557-573[CrossRef][ISI]
Thompson K. J. P. Grime 1979 Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology 67: 893-921[CrossRef]
Tuomi J. P. Nilsson M. Astrom 1994 Plant compensatory responses: bud dormancy as an adaptation to herbivory. Ecology 75: 1429-1436[CrossRef][ISI]
Weaver J. E. I. M. Mueller 1942 Role of seedlings in recovery of midwestern ranges from drought. Ecology 23: 275-294[CrossRef][ISI]
Whitham T. G. C. N. Slobodchikoff 1981 Evolution by individuals, plant-herbivore interactions, and mosaics of genetic variability: the adaptive significance of somatic mutations in plants. Oecologia 49: 287-292[CrossRef][ISI]
This article has been cited by other articles:
|
|
 |
|
  D. P. Belesky Regrowth Interval Influences Productivity, Botanical Composition, and Nutritive Value of Old World Bluestem and Perennial Ryegrass Swards Agron. J., February 7, 2006; 98(2): 270 - 279. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
