| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Biology, University of Mississippi, University, Mississippi 38677
Received for publication July 17, 1998. Accepted for publication February 1, 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: allocation • carnivorous plants • competition • fire • phenotypic plasticity • Sarracenia alata • Sarraceniaceae
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; McNaughton, 1979
; Dyer et al., 1982
; Jefferies, 1988;
Singh, 1993
; Brewer and Platt, 1994
). Two similar hypotheses, the herbivore-optimization hypothesis (McNaughton, 1979
; Dyer et al., 1982
) and the fire-optimization hypothesis (Daubenmire, 1968
; Hulbert, 1988;
Singh 1993
), predict that grazing or fire can increase the productivity of tolerant plants. In addition, grazing and fire generate repeated changes in the competitive environment experienced within the lifetime of tolerant long-lived plants. Although much work has focused on aboveground productivity of grazing-adapted and fire-adapted plants, much less is known about the ability of plants to exhibit morphological plasticity in response to changes in the competitive environment associated with disturbances of moderate intensity (but see Coughenour, McNaughton, and Wallace, 1985
; Brewer and Platt, 1994
). Such plastic responses are important, because they enable a plant to allocate resources optimally to different organs in such a way as to avoid or reduce the impact of competition from neighboring plants (Coughenour, McNaughton, and Wallace, 1985
; Slade and Hutchings, 1987
; Schmitt, 1993
; Brewer and Platt, 1994
; Dudley and Schmitt, 1996
).
Several authors have implied that fires increase the growth rate of fire-tolerant plants by reducing competition from neighboring plants and associated litter (Wallace, 1966
; Old, 1969
; Christensen, 1977
; Abbott and Loneragan, 1983
; Barker and Williamson, 1988
). Rarely, however, has this assumption been tested explicitly (Whelan, 1995
; but see Brewer et al., 1996
; Brewer, 1999
). Carnivorous plants such as pitcher plants (e.g., Sarracenia spp.) are ideal for examining the interacting effects of fire and neighbors on growth and plasticity. Pitcher plants are long-lived perennial plants with persistent rhizomes and are common in frequently burned seepage bogs. Therefore, an individual pitcher plant genet or ramet may experience variable competitive environments associated with recurrent fires during its lifetime. Curiously, although frequent fires are widely cited as playing an important role in maintaining populations of carnivorous plants in pine savannas (Wells, 1928
; Wells and Skunk, 1928
; Eleuterius, 1968
; McDaniel, 1971
; Schnell, 1976
; Weiss, 1980
; Folkerts, 1982
), few studies have employed appropriately controlled experiments to test the effects of fire or competition on the growth of carnivorous plants in pine savannas (but see Barker and Williamson, 1988
; Brewer, 1998b, 1999
). Further, the ability of carnivorous plants to alter patterns of allocation in response to fire-mediated changes in the competitive environment has rarely been examined (Weiss, 1980
).
In this study, I examine the interactive effects of fire and neighbors on growth and plasticity of the yellow pitcher plant, Sarracenia alata (Wood) Wood. Using phytometers (i.e., individual ramet transplants), I examine the immediate effects of fire, neighbors, and their interaction on ramet mass, the production of leaf traps (pitchers), and relative allocation of biomass to pitchers vs. belowground organs. I test the hypothesis that the negative impact of neighboring vegetation on phytometers is greater in years without fire. I hypothesize that pitcher plants are adapted to a range of fire frequencies and thus are capable of exhibiting fire-mediated plasticity in allocation to carnivorous function (i.e., the production of pitchers).
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Both adults and juveniles produce brightly colored (yellow or red) pitchers, which are open pitfall traps that capture insects. Pitcher plants are reported to absorb nutrients from the insects they capture and digest (Plummer and Kethley, 1964
; Christensen, 1976
). Pitchers are modified cataphylls or cataphyll-like leaves (i.e., leaves originating from scale-like, protective bracts surrounding the tips of rhizomes; Esau, 1977
). In S. alata, all mature cataphylls produce pitchers. No phyllodia (i.e., flattened cataphylls that do not form tubular pitchers at maturity) are produced in this species (Schnell, 1976
). Pitchers are produced primarily from March to October in open savannas in southern Mississippi (J. S. Brewer, personal observations). Emergence and growth of most pitchers, however, are usually completed by June. Although senescence of pitchers occurs throughout the year, most pitchers are moribund by December after the first frost in open savannas (Schnell, 1976
; J. S. Brewer, personal observations). Thus, few live pitchers are present during the winter months (i.e., January to March). The peak flowering time occurs from early March to late April, when solitary flowers are borne at the end of scapes.
Study area
My work was conducted in seepage bogs (pitcher-plant bogs sensu Folkerts, 1982
) within the University of Mississippi Forest Lands (UMFL) in Stone and George Counties in southeastern Mississippi. Seepage bogs are open, hydric pine savannas that occur downslope from mesic longleaf pine (Pinus palustris Mill.)-dominated uplands (Peet and Allard, 1993
; Olson and Platt, 1995
). They are maintained by a combination of hydric edaphic conditions, an impervious clay layer located near the surface, and frequent fires (1–3 times a decade), all of which are thought to reduce the establishment of trees (Streng and Harcombe, 1982
; Norquist, 1984
; Glitzenstein, Platt, and Streng, 1995
). The overstory of seepage savannas at UMFL is dominated by a sparse (
70–200 trees/ha) canopy of slash pine, Pinus elliottii, and to a lesser extent, longleaf pine. The understory contains a highly diverse mixture of perennial grasses, sedges, orchids, and low-growing monocots and forbs, including numerous carnivorous species such as Sarracenia spp., Drosera spp., Pinguicula spp., and Utricularia spp. A detailed description of species composition of the groundcover is provided in Peet and Allard (1993)
and Brewer (1998a)
.
Fire treatments
A field experiment was established at two sites, one of which was last burned in February of 1996 and the other in February of 1997. The current 2-yr study began in May 1996 and ended in May 1998. Therefore, for simplicity, the site last burned in February 1996 is hereafter referred to as the "unburned" site, whereas the site burned in February 1997 is hereafter referred to as the "burned" site. In other words, the burned site was burned during the course of the experiment (i.e., in February 1997), whereas the unburned site was not. Strictly speaking, however, both sites had been burned at the same frequency (once every 3 yr) since the early 1980s. In this way, I was able to examine short-term responses to a single fire, while controlling for the effects of fire frequency.
Although the effect of fire was not truly replicated in this study, I partitioned the effect of fire from other differences between the two sites by examining responses in two consecutive years at both sites (Fig. 1). Other than the year in which fires occurred, the two sites appeared similar to one another in most respects (e.g., fire frequency, tree density, pitcher plant density, area, standing crop, species composition; J. S. Brewer, unpublished data). In this study, the "effect of fire" is considered to be equivalent to the year x site interaction. Accordingly, the effect of fire could not be distinguished from other, unknown, causes of a year x site interaction.
|
; Brewer, 1999
). The effect of fire can be tested either by examining long-term effects of fire frequency (in which unburned sites represent a fire-suppression treatment) or by examining short-term responses to fire in a given year, while holding frequency constant. Studies that use long-unburned controls for the short-term effects of fire confound long-term effects of fire suppression with the short-term effects of a fire in a given year. Since the objectives of this study were to examine short-term responses to fire in a given year, both sites were burned at the same frequency but in different years. Therefore, the timing rather than the frequency of fire was manipulated.
Competition treatments
In the current study, competition is defined as a negative response of an individual plant to the presence of neighboring vegetation (see also Miller, 1996
). Thus, the intensity of competition was considered equivalent to the negative effect of neighbors on phytometer growth. At each of the two sites, 40 0.5 x 0.5 m plots were haphazardly located within patches dominated by herbs, >5 m from woody thickets near trees (see Brewer, 1998a
), and containing at least one pitcher-plant ramet. At each site, 20 replicate plots were randomly chosen to have all vegetation removed (-Neighbors), and the remaining plots were left as undisturbed controls (+Neighbors; Fig. 1). In early May 1996, 3 wk before transplanting, a short-lived, systemic herbicide, RoundupTM, was applied once at the recommended rate for herbaceous perennials (50 g/L; 1 L per plot) to the -Neighbors plots. One week later, all vegetation within these plots was clipped and cleared. The herbicide was very effective at killing most plants. Greater than 95% of the living stems were killed in the -Neighbors plots. The -Neighbors plots were repeatedly cleared of invading vegetation by hand throughout the study.
I predicted that the effect of neighbors on growth of pitcher plants would be greater at the unburned site than at the burned site, due to a fire-mediated reduction in the aboveground biomass of neighbors between the date of transplanting in the first year (May 1996) and the date of harvest in the first year (May 1997). During the first year, a fire occurred at the burned site but not at the unburned site. Conversely, the effect of neighbors was predicted to be similar at both sites between the date of transplanting in the second year (May 1997) and the date of harvest in the second year (May 1998). During the second year of the study, no fire occurred at either site. The null hypothesis was that there would be no significant year x site x neighbors interaction.
Phytometer selection
All phytometers were transplanted from a third site to control for average ecotypic and fire-related differences between the two sites into which they were transplanted. To ensure that phytometers had similar fire histories each year (i.e., all having been burned 3 mo earlier), a different site was used as a phytometer source each year. Therefore, ecotypic differences among phytometers were controlled only within a given year. In addition to site-related differences among phytometers, individual differences were controlled. Some researchers have argued that the benefit of producing pitchers varies with plant size (Gibson, 1983
; Givnish, 1989
; Cresswell, 1993
). Larger plants are better able to capture large flying insects than are smaller plants (Gibson, 1983
; Cresswell, 1993
; but see Newell and Nastase, 1998
). Presumably, if size is related to apparency, then the removal of neighbors artificially or by fire might increase the apparency of small plants to flying insects and increase capture rates (of small flying insects), thereby increasing growth rates. In other words, responses of small and large pitcher plants to competition may be asymmetric, whereby small plants benefit to a greater extent from competitive release than large plants (Keddy, Twolan-Strutt, and Shipley, 1997
).
To examine the role of phytometer size, I tested the effects of fire, neighbors, and their interaction on two different size classes of phytometers (Fig. 1). Consistent with the competitive asymmetry hypothesis, I predicted that small plants would benefit more from the release from competition than large plants and that these differences would be greater in a year without fire. The small size class included only those individual ramets whose largest pitcher had a diameter at its lip <1 cm. The large size class included only individual ramets whose largest pitcher had a diameter >2.5 cm. Ten replicate phytometers of each size class were assigned randomly to each competition treatment at each site in May 1996. In the following year, new phytometers were transplanted from a different recently burned site and randomly assigned to each competition treatment at each site in May 1997. The experimental design for this study was completely randomized and contained a factorial arrangement of site, year, neighbors, and size treatments with ten replicates within each of 24 or 16 treatment combinations.
Measurements
Differences in growth of phytometers were estimated by measuring final mass while controlling for differences in initial size. Upon transplanting in May of 1996 and 1997, an initial size of each phytometer was estimated by measuring the diameter of the largest pitcher at its lip. Diameter of the largest pitcher of plants from a recently burned site was highly correlated with ramet mass (r = 0.88, N = 20). In addition, live pitchers present at the time of transplanting were counted. Phytometers remained in the field for 1 yr and then were completely excavated. Total (i.e., both above- and belowground) dry mass of live tissue and the proportion of mass allocated to scapes and flowers, live pitchers (i.e., pitchers containing some visible pigment), rhizomes (and associated live immature cataphylls), and roots were measured for each phytometer. Live pitchers present at the time of excavation were counted.
I predicted that fire would reduce the effect of neighbors on growth (especially for small phytometers) by reducing differences in aboveground crops between +Neighbors and -Neighbors plots early in the growing season immediately following a fire. To examine whether fire interacted with the presence of neighbors to influence the aboveground crop of neighboring vegetation, leaf area index (LAI) was estimated within both +Neighbors and -Neighbors plots at both sites using a LI-CORTM (Lincoln, Nebraska) plant canopy analyzer. Measurements were taken at two different dates, June 1997 (4 mo after the 1997 fire, but early in the 1997 growing season), and September 1997 (late in the 1997 growing season but before late-season dieback). A previous study at the same sites indicated that LAI of groundcover at a recently burned site recovers to a level that is indistinguishable from the other site by 1 yr after a fire (Brewer, 1999
).
Statistical analyses
The effects of site, year, neighbors, size, and their interactions on total dry mass of phytometers were analyzed using four-way analysis of covariance (ANCOVA), wherein initial pitcher diameter was a covariate. In addition, the same analysis was used to examine treatment effects on the number of live pitchers present per plant at the time of excavation, using initial pitcher number as a covariate. One observation was excluded from these analyses because some of the plant material was lost during harvest. Although all phytometers survived the first 5 wk after transplanting, a total of 30 (out of 160) had died during both years of the experiment. The 30 dead and one missing phytometer that was lost during harvest were excluded from this analysis. Thus, conclusions regarding the effects of treatments on allocation patterns apply only to surviving phytometers. No assumptions of ANCOVA were violated, so no transformations of the data were necessary. Results of ANCOVA, wherein dead plants were assigned a value of 0 yielded the same conclusions, qualitatively (results not shown).
The effects of site, year, neighbors, size, and their interactions on the ratio of live pitcher mass to belowground mass and rhizome to root mass of phytometers were analyzed using four-way analysis of variance (ANCOVA). Initial diameter was the covariate. The 30 dead and the one missing phytometer were excluded from this analysis. Thus, conclusions regarding the effects of treatments on allocation patterns apply only to surviving phytometers. No assumptions of ANCOVA were violated, so no transformations of the data were necessary.
The effects of site, neighbors, and measurement date on LAI were examined using univariate repeated-measures ANOVA, wherein measurement date (with two levels, June 1997 and August 1997) represented the repeated-measures effect. Phytometer size was assumed to have a negligible effect on LAI and thus was ignored. Of particular interest was the three-way site x neighbors x measurement date interaction. LAI was log-transformed to reduce heteroscedacity. Analysis of variance and covariance tests were done using SUPERANOVA (version 1.11, Abacus Concepts, Inc., Berkeley, California, 1989).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
|
|
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Barker and Williamson, 1988
) that established pitcher plants derive an immediate benefit (in terms of net growth or productivity) from fire. The winter fire studied here removed dead leaves of pitcher plants and reduced the aboveground crop (both live and dead) of neighboring groundcover vegetation temporarily. This short-lived reduction in the aboveground crop of neighboring vegetation did not, however, stimulate faster growth rates in pitcher plants during this study. The lack of an immediate growth response to a single fire does not mean that pitcher plants would not benefit from recurrent fires over an extended period of time. If the intensity of competition were greater during prolonged fire-free intervals, then occasional fires might be necessary to maintain populations of S. alata in the long term. Both sites in the current study were burned at the same frequency (once every 3 yr). Woody vegetation was sparse at both sites and mostly restricted to dense thickets at the base of large pines (see Brewer, 1998a
). I have found previously that pitcher plants and other carnivorous plants rarely occur in woody thickets near trees (Brewer, 1998a, b
). Therefore, to the extent that long-term fire suppression results in encroachment of bogs by woody vegetation, pitcher plants could be negatively affected.
Although fire apparently had no immediate effect on the growth of established ramets of pitcher plants, a previous study has shown that fire increases reproductive success by increasing seedling establishment of S. alata (Barker and Williamson, 1988
). I did not examine seedling establishment in the current study. However, results of a companion study have confirmed Barker and Williamson's findings for seedlings and have revealed that fire increases early-seedling survivorship by consuming litter (S. Brewer, S. Laws, and A. Mozingo, unpublished data). Thus, as shown previously for another species of carnivorous plant, Drosera capillaris, effects of fire on survival and growth of pitcher plants may depend on the stage of the life cycle (Brewer, 1998b, 1999
).
In contrast to fire, competition reduces the growth rates of individual ramets of S. alata, even in the frequently burned bogs studied here, at least in some years. During the first year of the study, neighbors drastically reduced phytometer mass; their effects during the second year were much reduced. The cause of the differences in the intensity of competition between years is not known, but a late-summer drought that occurred in 1997 but not in 1996 likely reduced the impact of competition in the second year. The effect of neighbors was no greater at the unburned site than at the burned site, suggesting that, at least in bogs burned once every 3 yr, fire does not significantly release pitcher plants from competition. Not surprisingly, since fire did not reduce competition, there was no evidence of greater competitive asymmetry at the unburned site. In fact, neighbors appeared to have a greater effect on large plants than small plants. Regardless of whether neighbors were present, small plants appeared to be more vulnerable to mortality than large plants. Although previous studies have shown that winter fires increase the density of seedlings of carnivorous plants (either due to increased emergence from seed bank or increased young-seedling survival; DeBuhr, 1975
; Barker and Williamson, 1988
, Brewer, 1999
), after the earliest seedling stages, factors other than competition (e.g., soil disturbances) appear to become a relatively more important source of mortality of juveniles (Brewer, 1999
). Once established as adults, competition becomes important in reducing growth rates (Brewer, 1999
). The small phytometers of S. alata used in the current study were 2nd- to 3rd-yr juveniles, and thus were probably more vulnerable to mortality from sources other than competition.
Why would complete mortality of neighboring vegetation increase pitcher plant growth, whereas a fire would not? One possible explanation is that herbicide treatments reduce competition both above- and belowground, whereas fires primarily reduce competition aboveground. Given that seepage bogs are nutrient-poor habitats, one could argue that competition occurs primarily belowground (e.g., see Wilson and Tilman, 1993
). Another explanation is that herbicide treatments reduced competition for a greater period of time than did fire (Brewer et al., 1996
). Plants without neighbors likely benefited from reduced competition before the fire and for a long time after the fire, whereas intact neighboring vegetation recovered quickly following fire. Consequently, at the time of excavation, the aboveground crop was much greater in the burned plots with neighbors intact than in any of the plots without neighbors (Fig. 5).
Both fire and the removal of neighbors stimulate the production of pitchers
Although fire did not increase net total productivity of pitcher plants in this study, it did increase pitcher production and allocation to pitchers. This result agrees with findings of previous studies (e.g., Eleuterius, 1968
; Weiss, 1980
; Barker and Williamson, 1988
), which found that winter fires increased the production of foliage of pitcher plants. In addition, small pitcher plants appeared to produce a greater number of pitchers than large plants following fire (although effects on pitcher mass were not size dependent). My study highlights, however, how misleading it can be to assume that an increase in foliage production during the first year after a fire is equivalent to an immediate increase in the growth and vigor of pitcher plants. Rather, the fire-mediated shift towards greater allocation to pitchers documented here is more appropriately regarded as an example of phenotypic plasticity. Since all phytometers were obtained from the same site, significant variation in allocation patterns was associated with average differences in environmental conditions between sites and treatments. There is evidence for other species (e.g., Sarracenia purpurea) that pitchers are costly organs to produce (Dress et al., 1997
). Thus, a potentially important benefit of phenotypic plasticity is that pitcher plants are able to reduce allocation to costly pitchers in the presence of neighbors during years without fire. Therefore, rather than requiring frequent fires to persist, this species may be able to tolerate a relatively wide range of fire frequencies.
Shifts in allocation between pitchers and storage organs belowground potentially enable pitcher plants to increase investment in pitchers during periods when light is abundant and the effectiveness of leaf traps in prey capture is likely greatest, i.e., just after a fire (Gibson, 1983
). Even if prey capture is not greater after a fire, a cost-benefit model for carnivorous plants predicts that carnivory becomes less efficient as light becomes more limiting (Givnish et al., 1984
). There are several examples of carnivorous plants that reduce allocation to carnivorous function (e.g., via reduced allocation to attraction pigments) as the availability of light decreases (see Slack, 1979
; Givnish et al., 1984
; Givnish, 1989
; Zamora, Gomez, and Hodar, 1998
). I suggest that during fire-free years, pitcher plants respond to increasing aboveground competition by storing a greater fraction of resources belowground. Immediately after a fire, however, when light is less limiting and pitchers are potentially more apparent to prey (Gibson, 1983
), pitcher plants might benefit from converting these stored reserves into pitchers. The cost-benefit model mentioned above also predicts, however, that allocation to pitchers might decrease after a fire because of a short-term increase in the availability of nutrients in the soil (Givnish, 1989
). This prediction assumes that uptake by roots alone would be sufficient to sustain pitcher plants after a fire. Data from the current study indicate that pitcher plants decreased from their original size during the study. Final pitcher diameter (my best nondestructive estimate of ramet mass) was significantly lower than initial pitcher diameter (2.09 ± 0.156 cm SE (initial diameter) to 1.15 ± 0.129 cm SE (final diameter) in year 1; 1.856 ± 0.122 cm (initial diameter) to 1.53 ± 0.09 cm SE (final diameter) in year 2). Furthermore, data from a study of Sarracenia flava indicate that assimilation of phosphorus from captured prey may be necessary for the long-term persistence of genets (Weiss, 1980
). Thus, either storage, physiological integration of ramets within genets, or higher rates of prey capture are necessary to sustain individual ramets of pitcher plants. Uptake of nutrients by roots alone apparently is not sufficient to sustain individual ramets of pitcher plants. Phytometers were likely excavated too soon after the fire to determine whether fire-stimulated pitcher production resulted in increased capture rates and assimilation of prey-derived nutrients.
The responses of pitcher plants to neighbors and fire reported here suggest that individual ramets of pitcher plants "sit and wait" for periods of reduced aboveground competition occurring immediately after a fire to increase production of organs necessary for capturing both light and nutrients (pitchers). Such a foraging strategy is consistent with the hypothesis that a plant's abilities to compete for both light and nutrients are positively correlated (Grime, 1979
). Furthermore, a "sit and wait" foraging strategy parallels Grime's "stress-tolerator" strategy, in which growth is decoupled from the capture of resources in time and storage is critical to enduring prolonged shortages of resources. Sarracenia alata and some other carnivorous plants are unique, however, in that the same organ (a modified leaf) is primarily responsible for the capture of both light and nutrients. A comparison of foraging strategies of carnivorous and noncarnivorous plants could yield significant insight into the mechanisms of resource capture in plants.
|
FOOTNOTES |
|---|
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Barker, N. G., and G. B. Williamson. 1988 Effects of a winter fire on Sarracenia alata and S. psittacina. American Journal of Botany 75: 138–143.
Brewer, J. S. 1998a Patterns of plant species richness in a wet slash pine (Pinus elliottii) savanna. Journal of the Torrey Botanical Society 125: 216–224.[CrossRef][ISI]
———. 1998b Effects of competition and litter on a carnivorous plant, Drosera capillaris. American Journal of Botany 85: 1592–1596.
———. 1999 Effects of fire, competition, and soil disturbances on regeneration of a carnivorous plant, Drosera capillaris. American Midland Naturalist 141: 28–42.
———, and W. J. Platt. 1994 Effects of fire season and soil fertility on clonal growth in a pyrophilic forb, Pityopsis graminifolia (Asteraceae). American Journal of Botany 81: 805–814.[CrossRef][ISI]
———, ———, J. S. Glitzenstein, and D. R. Streng. 1996 Effects of fire-generated gaps on growth and reproduction of golden aster (Pityopsis graminifolia). Bulletin of the Torrey Botanical Club 123: 295–303.[CrossRef][ISI]
Christensen, N. L. 1976 The role of carnivory in Sarracenia flava L. with regard to specific nutrient deficiencies. Journal of the Elisha Mitchell Scientific Society 92: 144–147.[ISI]
———. 1977 Fire and soil-plant nutrient relations in a pine-wiregrass savanna of the coastal plain of North Carolina. Oecologia 31: 27–44.[CrossRef][ISI]
Coughenour, M. B., S. J. McNaughton, and L. L. Wallace. 1985 Responses of an African tallgrass (Hyparrhenia filipendula Stapf.) to defoliation and limitations of water and nitrogen. Oecologia 68: 80–86.[CrossRef][ISI]
Cresswell, J. E. 1993 The morphological correlates of prey capture and resource parasitism in pitchers of the carnivorous plant Sarracenia purpurea. American Midland Naturalist 129: 35–41.
Daubenmire, R. 1968 Ecology of fire in grassland. Advances in Ecological Research 5: 209–266.
DeBuhr, L. 1975 Observations of Byblis gigantea in southwestern Australia. Carnivorous Plant News 4: 60–63.
Dress, W. J., S. J. Newell, A. J. Nastase, and J. C. Ford. 1997 Analysis of amino acids in nectar from pitchers of Sarracenia purpurea (Sarraceniaceae). American Journal of Botany 84: 1701–1706.[Abstract]
Dudley, S. A., and J. Schmitt. 1996 Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. American Naturalist 147: 445–465.
Dyer, M. I., D. C. Detling, D. C. Coleman, and D. W. Hilbert. 1982 The role of herbivores in grasslands. In J. R. Estes, R. J. Tyre, and J. N. Brunken [eds.], Grasses and grasslands: systematics and ecology, 255–295. University of Oklahoma Press, Norman, OK.
Eleuterius L. N. 1968 Floristics and ecology of coastal bogs in Mississippi. Master's thesis, University of Southern Mississippi, Hattiesburg, MS.
Esau, K. 1977 Anatomy of seed plants, 2nd. ed. John Wiley & Sons, New York, NY.
Folkerts, G. W. 1982 The Gulf Coast pitcher plant bogs. American Scientist 70: 260–267.
Gibson, T. C. 1983 Competition, disturbance, and the carnivorous plant community in the southeastern United States. Ph.D. dissertation, University of Utah, Salt Lake City, UT.
Givnish, T. J. 1989 Ecology and evolution of carnivorous plants. In W. G. Abrahamson [ed.], Plant-animal interactions, 243–290. McGraw-Hill, New York, NY.
———, E. L. Burkhardt, R. E. Happel, and J. D. Weintraub. 1984 Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. American Naturalist 124: 479–497.[CrossRef][ISI]
Glitzenstein, J. S., W. J. Platt, and D. R. Streng. 1995 Effects of fire regime and habitat on tree dynamics in North Florida longleaf pine savannas. Ecological Monographs 65: 441–476.[CrossRef]
Grime, J. P. 1979 Plant strategies and vegetation processes. John Wiley & Sons, New York, NY.
Hulbert, L. C. 1988 Causes of fire effects in tallgrass prairie. Ecology 69: 46–58.[CrossRef][ISI]
Jefferies, R. L. 1988 Vegetational mosaics, plant-animal interactions, and resources for plant growth. In L. D. Gottlieb and S. K. Jain [eds.], Plant evolutionary biology, 341–369. Chapman and Hall, London.
Keddy, P., L. Twolan-Strutt, and B. Shipley. 1997 Experimental evidence that interspecific competitive asymmetry increases with soil productivity. Oikos 80: 253–256.[CrossRef][ISI]
McDaniel, S. 1971 The genus Sarracenia (Sarraceniaceae). Bulletin of the Tall Timbers Research Station 9: 1–38.
McNaughton, S. J. 1979 Grazing as an optimization process: grass-ungulate relationships in the Serengeti. American Naturalist 113: 691–703.[CrossRef][ISI]
Miller, T. E. 1996 On quantifying the intensity of competition across gradients. Ecology 77: 978–981.[CrossRef][ISI]
Newell, S. J., and A. J. Nastase. 1998 Efficiency of insect capture by Sarracenia purpurea (Sarraceniaceae), the northern pitcher plant. American Journal of Botany 85: 88–91.[Abstract]
Norquist, C. 1984 A comparative study of the soils and vegetation of savannas in Mississippi. Master's thesis. Mississippi State University, Mississippi State, MS.
Old, S. M. 1969 Microclimate, fire, and plant production in an Illinois prairie. Ecological Monographs 39: 355–384.[CrossRef]
Olson, M. S., and W. J. Platt. 1995 Effects of habitat and growing season fires on resprouting of shrubs in longleaf pine savannas. Vegetatio 119: 101–118.[CrossRef][ISI]
Peet, R. K., and D. J. Allard. 1993 Longleaf pine vegetation of the southern Atlantic and eastern Gulf Coast regions: a preliminary classification. In S. M. Hermann [ed.], Proceedings of the Tall Timbers Fire Ecology Conference, vol. 18, 45–81. Tall Timber Research Station, Tallahassee, FL.
Platt, W. J., G. W. Evans, and M. M. Davis. 1988 Effects of fire season on flowering of forbs and shrubs in longleaf pine forests. Oecologia 76: 353–363.[ISI]
Plummer, G. L., and J. B. Kethley. 1964 Foliar absorption of amino acids, peptides, and other nutrients by the pitcher plant, Sarracenia flava. Botanical Gazette 125: 245–260.
Schmitt, J. 1993 Reaction norms of morphological and life history traits to light availability in Impatiens capensis. Evolution 47:1564–1568.
Schnell, D. E. 1976 Carnivorous plants of the United States and Canada. John F. Blair, Winston-Salem, NC.
Singh, R. S. 1993 Effect of winter fire on primary productivity and nutrient concentration of a dry tropical savanna. Vegetatio 106: 63–71.[CrossRef][ISI]
Slack, A. 1979 Carnivorous plants. Ebury Press, London.
Slade, A. J., and M. J. Hutchings. 1987 Clonal integration and plasticity in foraging behaviour in Glechoma heteracea. Journal of Ecology 75: 1023–1036.
Streng, D. R., and P. A. Harcombe. 1982 Why don't east Texas savannas grow up to forest? American Midland Naturalist 108: 278–294.[CrossRef][ISI]
Wallace, W. R. 1966 Fire in the jarrah forest environment. Journal of the Royal Society of Western Australia 49: 33–44.
Weiss, T. E., Jr. 1980 The effects of fire and nutrient availability on the pitcher plant Sarracenia flava L. Ph.D. dissertation, University of Georgia, Athens, GA.
Wells, B. W. 1928 Plant communities of the coastal plain of North Carolina and their successional relations. Ecology 9: 230–242.[CrossRef][ISI]
———, and I. V. Skunk. 1928 A Southern upland grass-sedge bog. North Carolina Agricultural Experiment Station Technical Bulletin 32: 1075.
Whelan, R. J. 1995 The ecology of fire. Cambridge University Press, Cambridge.
Wilson, S. D., and D. Tilman. 1993 Plant competition and resource availability in response to disturbance and fertilization. Ecology 72: 599–611.
Zamora, R., J. M. Gomez, and J. A. Hodar. 1998 Fitness responses of a carnivorous plant in contrasting ecological scenarios. Ecology 79: 1630–1644.[ISI]
This article has been cited by other articles:
|
|
 |
|
  J. S. Brewer A demographic analysis of fire-stimulated seedling establishment of Sarracenia alata (Sarraceniaceae) Am. J. Botany, July 1, 2001; 88(7): 1250 - 1257. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
