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Effects of competition and litter on a carnivorous plant, Drosera capillaris (Droseraceae)¹

^a Department of Biology, University of Mississippi, University, Mississippi 38677

	ABSTRACT

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Although carnivorous plants are widely recognized as being generally restricted to open habitats, tests of the effects of competition on individual performance are extremely rare. In this study, I examined the effects of the removal of herbaceous and shrub canopies on seedling density and growth, survival, and reproduction of phytometers of a small insectivorous plant, Drosera capillaris (pink sundew). I also examined the distribution of this species in relation to the occurrence of woody species in a frequently burned wet savanna in southeastern Mississippi. Killing plants and removing dead biomass increased seedling density in both open areas and shrub thickets. The removal of dead biomass following herbicide application was critical to increasing densities of seedlings. Killing plants with herbicide without also clearing residual litter and standing dead was not sufficient to increase seedling densities in shrub thickets. Although the removal of the groundcover canopy strongly influenced the density of seedlings, it had very little effect on survival, growth, and reproduction of small phytometers during a single growing season. Survival of phytometers was greater in open areas than in shrub thickets, regardless of whether the groundcover canopy was removed. Densities of both seedlings and adults were greater in open areas away from shrub thickets than beneath the woody canopies of thickets and were negatively correlated with the leaf area index of groundcover vegetation. Results of this study show that the establishment of this carnivorous plant species is limited in part by the effects of litter on seedling density in both open areas and shrub thickets.

Key Words: carnivorous plants • competition • Drosera capillaris • Droseraceae • leaf area index • litter • shade

	INTRODUCTION

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Most carnivorous plants reside in open, wet, nutrient-poor environments (Givnish et al., 1984). In particular, nutrient-poor wet pine savannas and bogs of the coastal plain of the southeastern United States are characterized by an extraordinary abundance and diversity of carnivorous plants (Folkerts, 1982), perhaps only equaled in the tepuis of Venezuela and Guyana and in southwestern Australia (Givnish, 1989). There are two hypotheses to explain why carnivorous plants are largely restricted to open habitats. One hypothesis is that carnivorous plants are especially intolerant of shade because the benefit of producing costly leaf traps declines as light becomes more limiting, and thus photosynthesis becomes less efficient in shady environments (Givnish et al., 1984). A second hypothesis is that the effectiveness of leaf traps to attract prey is severely compromised when obscured by competing vegetation (Gibson, 1983). Regardless of the proximate cause, both hypotheses imply that carnivorous plants are poor competitors in dense vegetation compared to other types of plants.

Although numerous studies have implied that competing vegetation reduces the performance of carnivorous plants (Wells, 1928; Wells and Skunk, 1928; Eleuterius, 1968; McDaniel, 1971; Weiss, 1980; Folkerts, 1982; Gibson, 1983; Barker and Williamson, 1988; Givnish, 1989), explicit tests of the effects of competition are rare (see Wilson, 1985). Competition may inhibit the performance of carnivorous plants in a variety of ways. In noncarnivorous species, the presence of neighbors and their associated litter has been shown to inhibit seed germination and seedling survival (King, 1975; Werner, 1975; Sydes and Grime, 1981; Goldberg and Werner, 1983; Bergelson, 1990; Carson and Peterson, 1990; Facelli, 1994; Kitajima and Tilman, 1996). Effects of competition may change, however, with increasing age or size (e.g., see Grace, 1985; Platt and Weiss, 1985; Bergelson, 1990). To fully understand the mechanisms by which competition influences the success of carnivorous plants, it is critical to test the effects of competition on plants prior to and after establishment (Bergelson, 1990).

The competitive regime experienced by carnivorous plants of pine savannas is potentially greatly altered by fire. Fires occur frequently (more than once per decade) in pine savannas of the southeastern United States. Although most species of wet pine savannas are not killed by fire, fire is very effective at removing litter and standing dead, which might alter the competitive environment for low-growing carnivorous seedlings and rosettes of Drosera spp. In flammable grasslands and savannas, fire has been to shown to remove litter and thus increase seedling density of carnivorous (Barker and Williamson, 1988) and noncarnivorous plants (Kitajima and Tilman, 1996). Conversely, fires are generally less effective at removing litter in less flammable woody thickets or long-unburned pine-hardwood forests (Komarek, 1974). Consequently, examining the role that litter plays in inhibiting the emergence, growth, and establishment of carnivorous plants is relevant to understanding the relationship of carnivorous plants to fire in pine savannas.

In this study, I examined the effects of the removal of herbaceous and shrub canopies on seedling density and growth, survival, and reproduction of phytometers of a small insectivorous plant, Drosera capillaris Poiret (pink sundew). I also examined the distribution of this species in relation to the occurrence of woody species in a frequently burned wet savanna in southeastern Mississippi. I tested two hypotheses: (1) the removal of neighbors and their associated litter increases the density of seedlings of sundews, and (2) the removal of neighbors and their associated litter increases the growth, survival, and reproductive success of juvenile phytometers of sundews.

	MATERIALS AND METHODS

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Biology of Drosera capillaris
Pink sundews are small, rosulate, perennial insectivorous forbs, common in seepage savannas, bogs, and wet ditches in the coastal plain of the southeastern United States (Schnell, 1976). The peak flowering time for this evergreen species is during early to mid spring (April to May). Seedling emergence typically occurs from early winter to late spring and is stimulated by fire (author's observations and unpublished data).

Study area
This study was conducted in a wet pine seepage savanna at the University of Mississippi Forest Lands (UMFL) in Stone County in southeastern Mississippi. Seepage savannas 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; Platt, 1998). This savanna has been burned once every 3 yr since the early 1980s. It was last burned in February 1996. The site contains a second-growth stand of slash pine (Pinus elliottii Engelm.), and to a lesser extent longleaf pine, with a density of <200 individuals/ha. In addition, it contains a well-developed herbaceous groundcover community, with few signs of anthropogenic soil disturbances. The understory contains a highly diverse mixture of perennial grasses, sedges, shrubs, orchids, and scapose monocots and forbs, including numerous carnivorous species such as Sarracenia spp., Drosera spp., Pinguicula spp., and Utricularia spp. Species composition is similar to that previously described for "pine meadows" by Hilgard (1860), "pine barrens" by Harper (1914), and "southern longleaf savannas" by Peet and Allard (1993).

Effects of competition on seedling density
The effects of competition on seedling density were assessed by removing biomass and subsequently counting numbers of seedlings. In May 1996, I placed triplets of competition-treatment plots in open areas (>5 m from large trees) and within shrub thickets associated with slash pine trees. Within open areas, competition treatments were confined to 16 0.5 x 2 m plots each containing three adjacent 0.5 x 0.5 m quadrats. Within shrub thickets, treatments were confined to 14 triplets arranged haphazardly around the base of each of 14 randomly selected trees. Competition treatments were assigned at random to the three quadrats within each triplet. The three treatments included full competition (which was an undisturbed control), an herbicide application only (hereafter, herbicide), and an application of herbicide combined with a subsequent clipping and complete removal of all standing-dead vegetation (hereafter, no competition). A short-lived systemic herbicide, Roundup (Monsanto, St. Louis, Missouri) was applied once at the recommended rate for herbaceous perennials to both the herbicide and no-competition treatment quadrats. One week later, all vegetation within the no-competition treatment was clipped and cleared from these quadrats. The herbicide was very effective at killing most plants. More than 95% of the living stems were killed in both the herbicide and no-competition quadrats.

The purpose of assigning two different types of competition-reduction treatments was to test the inhibitory effect of the aboveground standing crop and associated litter minus the active uptake of soil resources and continued growth of established plants. Two planned orthogonal contrasts were done to examine the effect of different levels of competition on seedling density. The first contrast, "no competition vs. competition," compared the average response to the full competition and herbicide treatments with the response to the no-competition treatment. The second contrast, "Full competition vs. herbicide," compared the response to competition with live and dead plants (full competition) with the reponse to competition with dead plant material only (herbicide treatment).

In mid-December 1996, all quadrats in open areas and shrub thickets were censused for seedling and adult density. I considered "seedlings" to be all plants containing cotyledons or small juveniles containing no more than four primary leaves, with a rosette diameter no greater than 5 mm. Established adults are frequently greater than 10 mm in diameter (Radford, Ahles, and Bell, 1968). I used split-plot ANOVA to test the fixed effects of microsite (i.e., open area vs. thicket, whole-plot effect) and competition (split-plot effect) on seedling densities. Density was natural-log transformed to reduce variance heterogeneity among treatments.

Effects of competition on the performance of phytometers
To examine the effect of competition on postemergent plants, I measured the survival, growth, and reproduction of phytometers transplanted into ten randomly chosen replicates of the abovementioned competition plots in open areas and thickets. Phytometers were seedlings and small adults (<7 mm in diameter) excavated from a wet ditch in a fire break at the border of the site. Ten phytometers were transplanted into each quadrat. Prior to transplantation, initial sizes of all phytometers were determined by measuring rosette diameter. All phytometers were first permanently marked with strips of wire. Subsequent censuses of density and survivorship were conducted in these quadrats in mid-May and early August in 1997. Repeated-measures, split-plot ANOVA was used to test how the effects of microsite (whole-plot) and competition (repeated-measure treatment) on phytometer density changed over time (from May to August 1997, i.e., the split-plot census effect). During the May census the reproductive status of all individuals was determined. Reproductive status was determined by noting the presence of a scape. Growth rates were estimated in the August census by measuring rosette diameter in August and calculating a relative growth rate [RGR; ln(diameter_August) - ln(diameter_May)].

Effects of microsite on density and groundcover leaf area index
To quantify differences in sundew densities between open areas and shrub thickets, numbers of sundews (seedlings and adults) were counted in full competition quadrats in open areas and shrub thickets in December 1996. The effect of microsite on log densities of sundews was analyzed using analysis of covariance (ANCOVA). An estimate of the aboveground standing crop of the groundcover vegetation (i.e., excluding large trees), leaf area index (LAI), was used as a covariate. A LI-COR (Lincoln, Nebraska) plant-canopy analyzer was used to quantify differences in LAI between full-competition quadrats in open areas and in shrub thickets during May 1997. Differences in LAI between open areas and shrub thickets were tested using two-sample two-tailed t tests, assuming unequal variances. Analysis of variance tests were done using SuperAnova (Abacus Concepts, Inc., Berkeley, California), while t tests were done using StatView (Abacus Concepts, Inc., Berkeley, California).

	RESULTS

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Effects of microsite, herbicide, and the removal of residual litter on seedling density
Seedling density was an order of magnitude higher in open areas than in shrub thickets (Fig. 1; microsite main effect, F_1,28 = 52.54, P < 0.0001). Aboveground standing crop and associated litter greatly inhibited seedlings in both open areas and thickets within the savanna (Fig. 1; treatment main effect, F_2,56 = 38.57, P < 0.0001). At both microsites, more of the inhibitory effect could be attributed to standing dead and associated litter than to live vegetation (Fig. 1, Table 1; compare contrasts). This was especially true within shrub thickets (Fig. 1). Consequently, there was a significant microsite x treatment interaction (F_2,56 = 4.98, P = 0.01). In shrub thickets, seedling density was significantly greater in the no-competition treatment than in the full-competition and herbicide-only treatments (P < 0.0001), whereas seedling density did not differ significantly between full-competition and herbicide-only treatments (P = 0.5, Table 1).

View larger version (38K): [in this window] [in a new window]   Fig. 1. Effects of competition treatment on seedling density in two microsites. Error bars are ± 1 SE.

View larger version (19K): [in this window] [in a new window]   Fig. 2. Changes in phytometer density over time in two microsites. Error bars are ± 1 SE.

Effects of microsite on sundew density and leaf area index
Densities of all sundews (seedlings and adults) were greater in open areas than in shrub thickets (least squares mean [i.e., adjusted mean] = 1.427 + 0.145 SE vs. 0.322 + 0.158 SE for open areas and shrub thickets, respectively; F_1,27 = 19.93, P < 0.0001) and were negatively correlated with LAI (r = -0.51, F_1,27 = 5.72, P = 0.024). LAI was greater in shrub thickets than in open areas (2.2 + 0.19 SE vs. 1.14 + 0.09 SE, respectively; t₁₉ = 5.10, P < 0.0001).

	DISCUSSION

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Competition influences the performance of pink sundews primarily by reducing the density of seedlings. The inhibitory effect of established vegetation on the density of seedlings of sundews in undisturbed areas appears to be caused more by live vegetation than by standing dead and associated litter. The increased inhibition caused by live vegetation is likely due to the additional effects of belowground competition that live plants exert. The relatively small additional inhibition caused by live vegetation compared to that caused by standing dead and litter, however, suggests that aboveground competition may be more important than belowground competition at limiting seedling density (especially within shrub thickets near trees). Increased establishment of seedlings following the removal of standing dead and litter may be an adaptive response to fire, given that fires cause very little mortality of established herbaceous plants, but remove most litter and standing dead. The inhibition of seed germination or early-seedling survivorship by shading (or possibly allelopathic compounds) may be an important mechanism of competition. Numerous studies have previously demonstrated that both litter and live established plants inhibit germination or increase seedling mortality (e.g., King, 1975; Werner, 1975; Sydes and Grime, 1981; Goldberg and Werner, 1983; Bergelson, 1990; Carson and Peterson, 1990; Facelli, 1994; Kitajima and Tilman, 1996; Foster and Gross, 1997). Germination rates of seeds of sundews and other carnivorous plants are typically greater under well-lit conditions (Schnell, 1976). Furthermore, fire appears to be important in stimulating germination of carnivorous species (DeBuhr, 1975; J. S. Brewer, unpublished data). Disturbance-stimulated germination may enable sundews to take advantage of recently disturbed or burned habitats. Alternatively, preliminary studies of another carnivorous genus, Sarracenia spp. (which exhibits higher seedling densities after a fire; Barker and Williamson, 1988) reveal that equal rates of germination occur in the dark and under well-lit conditions (J. S. Brewer, S. Laws, and M. Mozingo, unpublished data). Thus, lower seedling densities at high-litter sites may simply reflect higher rates of early-seedling mortality immediately following germination (Bergelson, 1990). In either case, pink sundews exhibit characteristics of ruderal species (sensu Grime, 1979) that are relatively poor competitors in dense vegetation.

Although the density of seedlings of sundews was greatly reduced by competing vegetation, survival, growth, and reproduction of small phytometers were little affected by the removal of groundcover vegetation in the first growing season after transplantation. These results were unexpected and appear to be inconsistent with the hypotheses that carnivorous plants are shade intolerant (Givnish et al., 1984) or capture fewer prey in dense canopies (Gibson, 1983). I caution, however, that this experiment did not provide an adequate test of either hypothesis for at least three reasons. First, the removal of groundcover vegetation might not have substantially altered light levels. For example, the no-competition treatment had no effect on the amount of shade cast by the large trees with which shrub thickets were associated. In fact, differences in light levels near and away from trees might explain the lower survival rates of sundews near trees, regardless of the competition treatment. Such a response is consistent with the hypothesis that sundews are shade intolerant (Givnish et al., 1984). Second, since phytometers were relatively small (i.e., on average, 5 mm in diameter), it is possible that they were not large enough to attract prey, and thus, the additional light or prey potentially made available by the removal of groundcover vegetation might have had little affect on growth, survival, or reproduction (Gibson, 1983; Givnish et al., 1984). There is evidence from another study (J. S. Brewer, unpublished data) that large sundews do benefit from the removal of neighbors. Third, more than a single growing season may be required before competition from groundcover vegetation inhibits the growth and reproduction of established plants. Clearly, additional experiments are necessary to adequately test the shade-intolerance and prey-attraction hypotheses of Givnish et al. (1984) and Gibson (1983), respectively.

In conclusion, competition influences the performance of pink sundews in complex ways. Competition from groundcover vegetation and standing dead strongly affects the reproductive success of sundews by limiting colonization, germination, or early-seedling survival. Pink sundew appears to be an opportunistic species, capable of taking advantage of recently disturbed conditions. Results from this study further show, however, that competition does not necessarily have the same effects on all stages of the life cycle of this species. Once seedlings of pink sundews reach a sufficiently large size (e.g., 5 mm in diameter), survival appears to be little affected by competition from groundcover vegetation (at least in the short term), although shading by trees may be important. Additional experimental work is needed to determine the responses of established adults to competition.

	FOOTNOTES

 
¹ The author thanks Allen Albritton; the staff of the University of Mississippi Forest Lands for technical assistance and for administering the prescribed burns, Jill Balducci, Edgar Leighton, Micah Walker, and Steven Ashley for assistance in the field, and Joy Bergelson, Carl von Ende, and Aaron Ellison for their constructive critical reviews of this manuscript. Support for this project was provided by a grant from the University of Mississippi Small Grants/Faculty Summer Support program.

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