Bison Increase the Growth and Reproduction of Forbs in Tallgrass Prairie.
In many grassland ecosystems, the activities of large vertebrate grazers strongly influence the physiology, growth, life history patterns, and population dynamics of plants. Large grazers also play an important role in shaping grassland plant community structure, floristic diversity, and patterns of net primary productivity (Bakker et al., 1983; Karki et al, 2000; Koerner and Collins, 2013; Milchunas and Lauenroth, 1993; McNaughton, 1985). The consumption of plant tissue and the other activities of large grazers also alter grassland habitats in ways that strongly affect other consumers such as insects, birds, and small mammals. (Joern, 2005; Moran, 2014; Powell, 2006).
In North American tallgrass prairies, large grazers such as bison can influence plant communities in many ways: by altering nutrient cycling (Johnson and Matchett, 2001), removing biomass (Knapp and Seastedt, 1986), creating disturbances through activities such as wallowing and trampling (Knapp et al., 1999), and altering the patterns of other disturbances such as fire. At the plant community level, the presence of bison or cattle at low to moderate densities has been shown to increase overall plant species diversity relative to ungrazed prairie, with most of the additional species being forbs (Collins et al, 1998; Hartnett et al., 1996). Although grasses are responsible for the majority of annual net primary produc tivity in tallgrass prairie, forbs (dictotyledonous herbs) comprise the majority of the ecosystem's floristic diversity (Towne, 2002).
The mechanisms by which bison increase plant diversity are not yet fully understood. One proposed explanation is the competitive release hypothesis. This posits the reduction in cover and biomass of graminoids due to consumption by grazers increases resource availability (particularly light) and reduces the competitive effects of dominant grasses on subdominant and subordinate forb species, increasing their relative abundance. Both bison and cattle preferentially feed on graminoids and tend to avoid consuming most annual and perennial forbs (Hartnett et al., 1997; Knapp et al, 1999). Therefore, reduction of competitive pressure from grasses may contribute to increases in the performance and density of forb species that are suppressed by competition when bison are absent, leading to the observed increase in diversity. The increase in prairie grass cover and biomass in the absence of large grazers also suggests competitive pressure from grasses may inhibit the survival of many native prairie species when grazers are not present (Koerner and Collins, 2013).
A second proposed mechanism explaining increased plant species diversity in grazed grasslands is the habitat heterogeneity hypothesis. Patchy grazing and other activities of bison such as wallowing, trampling, and dung and urine deposition have been shown to increase local habitat heterogeneity, and this increase in patchiness and diversity of microhabitats may explain the higher plant species richness found in bison-grazed prairies (Steinhauer and Collins, 1995; Hartnett et al, 1996; Knapp et al, 1999). Grazers also tend to increase the amount and patchiness of bare ground, opening up space for lateral spread of clonal species and safe sites for plant recruitment from seed or buds (England and DeVos, 1969). Under the interacting disturbances of periodic fire and grazing in tallgrass prairie, frequent fire tends to decrease plant community heterogeneity, whereas bison offset this decline and maintain high heterogeneity (Collins et al., 1998; Knapp et al., 1999). Studies in both North American and southern African grasslands have shown that, when large grazers are removed, both community heterogeneity and plant species richness decline (Collins et al, 1998; Eby et al., 2014; Knapp et al., 1999).
These two mechanistic hypotheses are not mutually exclusive. In grasslands where large grazers are present, their effects on plant competitive interactions are often complemented by effects of patchy physical disturbances such as trampling, wallowing, and dung and urine deposition and both may operate to generate the observed increase in plant species diversity. They differ in that the habitat heterogeneity hypothesis predicts an increase in forb species richness, but not necessarily mean forb performance (individual plant growth and reproduction), whereas the competitive release hypothesis also predicts an increase in forb performance.
At the individual plant level, both tissue consumption and alteration of local habitats by large herbivores may affect various aspects of plant life history such as growth, biomass allocation patterns, survival, and the amount, timing, and mode of reproduction (Noy-Meir, 1993; Pastore and Russell, 2012). According to optimal partitioning theory, individual plants alter their growth plasticity and biomass allocation in response to changes in resource limitation, maximizing fitness by allocating a higher percentage of resources to the growth of structures whose functions are particularly important in a given environment (Bazzaz et al., 1987; Chapin et al., 1991; McCarthy and Enquist, 2007). For example, local light limitation may cause an individual to increase biomass allocation to stem to compete with neighbors by increasing height (De Kroon et al, 2009), whereas soil nutrient limitation may cause increased carbon allocation to root growth or to supporting mycorrhizal symbionts. Unlike many other ecosystems that are shaped by a single limiting resource, a distinguishing characteristic of tallgrass prairie is limiting resources are temporally and spatially variable, such that the most limiting resource switches over time and among local patches (Seastedt and Knapp, 1993; Blair, 1997). Therefore, we predict phenotypic plasticity in biomass allocation patterns in tallgrass prairie plants should be high, differing significantly between habitats with and without large herbivores. It is important to increase our understanding of the link between environment and plant life history patterns since, over time, widespread alterations in life history in response to environmental pressures can cause changes in population and community dynamics.
Our first objective of this study was to test predictions of the competitive release hypothesis that the presence of large grazers (bison) on tallgrass prairie reduces canopy density, increases available light, and increases the growth, reproduction, and cover of forb species. Our second objective was to test the hypothesis perennial forbs show high phenotypic plasticity in biomass allocation patterns in response to bison-induced alterations in habitat and increased resource availability. We specifically predicted forbs grown in habitats where bison are present would generally show larger total biomass, lower allocation to stem, higher allocation to reproduction, and higher allocation to vegetative versus seed reproduction compared to conspecifics grown in habitats without bison.
MATERIALS AND METHODS
SITE AND SPECIES DESCRIPTIONS
This study was conducted at Konza Prairie Biological Station (KPBS), a 3487-ha tallgrass prairie preserve jointly owned by the Nature Conservancy and Kansas State University. KPBS is located in the Flint Hills ecoregion of Kansas (39[degrees]05'N, 96[degrees]35'W), which is characterized by a continental climate with average monthly temperatures ranging from -2.7 to 26.6 C. Average annual precipitation at KPBS is 835 mm, approximately 75% of which falls during the growing season (Knapp et al, 1998; LTER dataset AWE012). Between Apr. 1 and Oct. 31 of 2013, the year of this study, approximately 672 mm of precipitation fell and temperatures ranged from -4.3 to 39.7 C with an average of 19.4 C.
KPBS is subdivided by watershed into numerous fire (burned every 1, 2, 4, or 20 y since 1972) and grazing management regimes (ungrazed, grazed by bison, grazed by cattle). Bison have been present in the native grazer treatments since 1987, allowing for the study of the long-term impacts of bison on plant communities (Knapp et al, 1998). The vegetation of KPBS consists primarily of unplowed native tallgrass prairie dominated by warm-season perennial [C.sub.4] grasses such as big bluestem (Andropogon gerardii Vitman), little bluestem (Schizachyrium scoparium Michx.), and Indiangrass (Sorghastrum nutans L.). Subdominant vegetation includes a diverse mix of forbs, cool-season [C.sub.3] grasses, and a few woody species. Over 576 species of vascular plant have been identified at KPBS representing over 96 plant families, but >40% of species belong to the families Poaceae, Asteraceae, Fabaceae, and Cyperaceae alone (Towne, 2002). This study, conducted in 2013, measured the growth, biomass allocation patterns, and reproduction of six common perennial forb species representing replicate populations in watersheds with and without large grazers (bison). All watersheds used in this study have been burned at 2-y intervals for more than 2 dec but had not been burned in the year of this study. None of the species chosen for this study are considered palatable to large ungulate grazers. Ambrosia psilostachya DC., Artemisia ludoviciana Nutt., Vernonia baldwinii Torr., and Solidago canadensis L. are all rhizomatous representatives of the family Asteraceae. The rhizomatous Baptisia australis (L.) R. Br. and nonrhizomatous Psoralidium tenuiflorum (Pursh) Rydb. are both members of the family Fabaceae. These two families are the most abundant and diverse families of forbs on tallgrass prairie.
FIELD SAMPLING AND PLANT MEASUREMENTS
For each species, six populations on similar topographical positions were randomly selected for sampling, three in the bison-present treatment and three in the bison-absent treatment. Within each population, a transect was randomly placed and 12 individuals were selected at randomly chosen intervals of at least 2 m. Therefore, a total of 72 individuals of each species were sampled (36 in bison-present habitats and 36 in bison-absent habitats). The three populations sampled in the bison-present treatment were located in watershed N2A, but the populations sampled in the bison-absent treatment were split between the watersheds 2A and 2B at KPBS. Each individual was marked with a flag and metal tag in early May and followed throughout the growing season until it reached peak flower. An individual was defined as a single ramet for A. psilostachya, A. ludoviciana, S. canadensis, and V. baldwinii. For B. australis and P. tenuiflorum, an individual was defined as the marked stem and all living connected stems. If a marked individual died (or senesced prematurely), the nearest conspecific was chosen as a replacement and the death was noted. No signs of bison herbivory were observed on any individuals marked for use in this study.
For each species individuals were harvested when they reached peak flower or, in the case of vegetative individuals, when all neighboring individuals were at peak flower and no sign of reproductive development was discernible. Whether each harvested individual was reproductive or vegetative was recorded. Since it is nonclonal, P. tenuiflorum was harvested by clipping stems at soil level, but all other species were excavated to collect underground vegetative reproductive structures. Harvesting root biomass was impossible in Konza's rocky, clay soil, but every effort was made to remove all rhizomes associated with each individual. Ultimately, 29-36 individuals per treatment were harvested for each species.
After harvest, the aboveground portions of each plant were dissected into three main functional components: stems, leaves, and sexual reproductive structures (including flowers, bracts, and some peduncles/rachises). All parts of the plant were then oven-dried at 60C for at least 72 h, then weighed to the nearest 0.001 g. Only live tissues were sampled, dried, and weighed. Since herbivorous insects consumed a substantial quantity of the flowers and developing fruits of B. australis, making it impossible to determine the true weight of sexual reproductive structures, the mass of floral stems (rachis/peduncle) was used as an approximation of reproductive biomass for this species. The number of flowers or fruits (or floral nodes in the case of B. australis) produced by each individual was also determined during dissection as an estimate of potential fecundity for each species except S. canadensis. Herbivorous insects also consumed many flowers of P. tenuiflorum, and only nondamaged fruits and flowers were counted for this species since that represents a more accurate estimate of functional fecundity than a count that included unviable flowers or fruit, and any potential bison-mediated differences in insect herbivory would be relevant to the survival and fecundity of this species. Percent allocation to stem, leaves, and reproduction were determined by dividing their mass by total aboveground biomass for each individual. The stem:leaf biomass ratio was also calculated. For each species, one-way ANOVA was used to determine whether percent allocation to any one function, or stem:leaf ratio differed between populations in habitats with and without bison. For the percentage values, the test was run using a beta-distribution.
Of the five rhizomatous species studied, only three species had rhizomes that were sufficiently developed by time of harvest for analysis: B. australis, S. canadensis, and V. baldwinii. For each species, all developing rhizomes associated with each harvested individual were counted, excised, and collected. The rhizomes were then oven-dried at 60C for at least 72 h, then collectively weighed to the nearest 0.001 g to attain the total mass of rhizomes per individual. The ratio of rhizome biomass to total aboveground biomass was calculated for each individual as an assessment of proportional allocation to vegetative reproduction. For each species, one-way ANOVA assuming a beta-distribution was used to determine whether proportional allocation to vegetative reproduction differed between habitats with and without large grazers.
Plant size was measured in three ways: plant height, total aboveground biomass, and total number of leaves produced. Each individual's height was measured to the nearest 0.5 cm at peak flower, or, for vegetative individuals, after all neighboring conspecifics had reached peak flower. Total aboveground biomass was determined for each plant as the sum of the dry weights of all aboveground parts. For many plants, older leaves had senesced and been shed prior to sampling; therefore, total number of leaves produced was determined by counting the number of nodes. The exception was A. ludoviciana which did not shed older leaves, allowing the total number of leaves present to be counted as a direct measure of leaf production. For each species, one-way ANOVA was used to test for significant differences in height, total aboveground biomass, and number of leaves between populations with bison present versus bison-absent.
In order to better understand the differences between prairie habitats with and without the presence of large grazers, aspects of the vegetation surrounding each individual such as vegetation density, light interception, plant heights, and ground cover were measured. Vegetation density was estimated by measuring disk settling height (cm) of a pasture disk meter at 10 randomly chosen locations near each transect during peak overall biomass in August. The pasture disk meter is a common nondestructive tool for measuring vegetation density since there is typically a strong positive linear relationship between disk settling height and vegetation density in grassland communities (Bransby and Tainton, 1997; Karl and Nicholson, 1987; Sharrow, 1984). For this study, linear regressions between aboveground biomass and disk settling height previously determined for tallgrass prairie at KPBS by Trollope et al. (2002) were used to estimate aboveground vegetation density (Biomass density in kg/ha= 1805 [Vdisc settling height in cm] - 2065). An AccuPAR LP-80 ceptometer (Decagon Devices, Pullman, Wash.) was used to measure photosynthetically active radiation ([micro]mol x [m.sup.-2] x [s.sup.-1]) above the canopy, at the top of each sampled individual, and at ground-level near each marked individual (but outside of the shade of the individual itself). For each plant light was measured five times at each of those three positions. The light available to each plant sampled could therefore be quantified by calculating the average percentage of ambient light available at the top of the plant and at ground-level. All light measurements were taken within 1 h of solar noon on clear days.
Percent canopy cover and species richness of neighbors was measured within a 0.5-[m.sup.2] plot centered around each marked individual. Percent cover of forbs, grasses, shrubs, conspecifics (including the individual studied), and bare ground were estimated using a modified Daubenmire method (Daubenmire, 1959). For each measurement, canopy cover was determined to be closest to the midpoint of one of seven classes: 0-1%, 1-5%, 5-25%, 25-50%, 50-75%, 75-95%, or 95-100%. Species richness of forbs and shrubs was also estimated within each plot, but grass richness was not measured due to the difficulty of identifying vegetative grass tillers. Mean species richness per transect was calculated for each site.
One-way ANOVA was used to determine whether percent light availability, canopy height, nongraminoid plant species richness, vegetation density (disk settling height), or percent canopy cover were significantly different between habitats for individuals of each species. For the percentage values, the test was run using a beta-distribution.
In tallgrass prairie habitats grazed by bison, the abundance (canopy cover) of competing grasses was much lower relative to habitats without bison. In habitats with bison, the canopy cover of grasses was significantly lower (P < 0.0001), forb canopy cover was significantly higher (P < 0.0001), and the area of bare ground was several times higher than in habitats without bison (P < 0.0001; Fig. 1a). Similarly, the overall aboveground vegetation density (as estimated from the disk pasture meter) was significantly lower in habitats grazed by bison (P < 0.0001; Fig. lb). As a result, the percentage of ambient light (PAR) measured at the top of the sampled forbs was significantly higher in habitats with bison than habitats without bison, and the percentage of ambient PAR reaching ground level was more than three times higher in habitats with bison (P < 0.0001 for both; Fig. 1c).
For all six forb species and in all sites studied, nongraminoid species richness in the local neighborhood was two times greater in sites with bison than in sites without bison and the difference between sites was statistically significant (P < 0.001; Fig. Id). Several measures of forb growth and reproduction were consistently higher among plants growing in habitats with bison than in habitats without bison. In four of the forb species (A. psilostachya, B. australis, V. baldurinii, and S. canadensis) total aboveground plant biomass was significantly higher in sites with bison present (Table 1). The other two species (A. ludoviciana and P. tenuiflorum) showed very similar trends, but the differences between habitats were not significantly different (Table 1). In B. australis, S. Canadensis, and V. baldurinii, larger plant size (biomass) in habitats with bison was also reflected in a significantly larger number of leaves produced in habitats with bison relative to habitats without large grazers (Table 1). Although the biomass of plants in habitats with bison was significantly higher, there was no clear pattern of differences in height between plants in habitats with and without bison (Table 1). In four of the six species, a higher percentage of plants flowered in habitats with bison than in sites without bison, and in five of the six forb species, total reproductive biomass was significantly higher in habitats with bison (Table 1). Most of the forb species showed similar trends in aboveground biomass allocation patterns, with plants in sites with bison showing generally lower biomass allocation to stems, higher biomass allocation to reproduction (reproductive effort), and no change in allocation to leaf tissue relative to plants in sites without bison (Fig. 2). The increase in reproductive allocation in bison-grazed habitats was statistically significant for five of the six species (A. psilostachya, P. tenuiflorum, B. australis, S. canadensis, and V. baldurinii), and the decrease in allocation to stem was statistically significant in four of the species (A. psilostachya, P. temiijlorum, S. canadensis, and V. baldwinii; Fig. 2). In five of the six forb species, there was no significant difference in biomass allocation to leaves between habitats. Only A. psilostachya allocated significantly less biomass to leaves in habitats without bison. In the three species that reproduce vegetatively as well as by seed, only S. canadensis showed a significant response to the habitat difference, with significantly lower vegetative reproductive effort (biomass allocation to rhizomes) in habitats with bison present (Table 2). In both B. australis and V. baldwinii, there was no significant difference in vegetative reproductive effort between habitats, although both of these species produced a significantly larger number of rhizomes in habitats with bison (Table 2).
Competition for light appears to be significantly reduced in habitats with bison. The percentage of ambient PAR incident on forbs and at ground-level was much higher in habitats with bison, indicating greater overall light availability for individuals. Lower neighborhood vegetation density and canopy height in habitats with bison also indicates reduced competition for light. Habitats with bison also showed changes in the local neighborhood environment of the individuals studied. The species richness and cover of nongraminoids (forbs and few shrubs) and amount of bare ground was consistently higher and graminoid cover was much lower in habitats with bison than in habitats without large grazers. Increased forb cover and species richness in habitats where bison are present is consistent with the findings of previous studies (Collins et al, 1998; Hartnett et al, 1996; Hickman et al., 2004). The greater availability of bare ground in habitats with bison suggests a greater availability of safe sites for new seedling or ramet establishment by subdominant or understory forbs. Taken together the differences in light availability and ground cover indicate two distinctly different aboveground environments for forbs. In the absence of bison, forbs compete predominantly with the strongly dominant tall grasses, which significantly decrease the availability of light and bare ground. In habitats altered by bison, forbs are surrounded by a much less dense canopy composed of a more diverse array of smaller neighbors, and they experience less light and space limitation. Though the belowground environments were not measured, the two habitats may also differ in nutrient availability, soil moisture, soil microbiota, and soil temperature, but these differences would not generally be expected to decrease forb performance in habitats with bison (Fahnestock and Knapp, 1994; Frank and Groffman, 1998; Hobbs, 1996; Knapp and Seastedt, 1986; Knapp et al., 1999; Veen et al., 2014; Wilson et al., 2001).
PLANT GROWTH AND REPRODUCTION
For four out of six species, individual plant size was significantly greater in habitats with bison according to at least one measure. In habitats with bison, individual forb aboveground biomass was generally greater, as were the number of leaves. This increased growth supports the hypothesis the presence of bison increases forb performance in tallgrass prairie. Plant height showed no consistent differences between habitats. Light limitation typically causes plants to produce longer internodes, so the lack of a consistent difference in height despite other evidence of reduced growth in habitats where bison are absent suggests light limitation is important in constraining forb performance in ungrazed prairie habitats (Dudley and Schmitt, 1996; Harper, 1977; Lockhart, 1964). The two species that showed no differences in size (A. ludoviciana and P. tenuiflorum) may be less plastic in their growth or may be less sensitive to the environmental differences between bison-grazed and ungrazed prairie habitats. Nevertheless, the fact that four species showed increased size in terms of biomass and/or module number in habitats with bison provides evidence that competition for resources (particularly light) is reduced by the activities of bison.
At least one measure of sexual reproduction was greater in habitats with bison for all six species. For all species except P. tenuiflorum, individuals in habitats with bison were significantly more likely to flower. Number of flowers was greater for three out of the five species for which numbers were available, and mass of reproductive structures produced per individual was greater for all species except A. ludoviciana. Number of flowers and mass of sexual reproductive structures can be interpreted as estimates of fecundity since they are generally allometrically related to the number of seeds produced in the absence of mitigating factors such as seed predation. Sexual reproductive effort (the biomass fraction in reproductive structures) was greater in habitats with bison for all species except A. ludoviciana. Therefore, not only were a greater percentage of forbs reproductive in habitats with bison, they were also generally more fecund, resulting in much greater sexual reproductive output in habitats with bison.
Vegetative reproduction did not show a clear pattern of difference between habitats in the three species in which it was studied (B. australis, 5. canadensis, and V. baldwini). There was no significant difference in total rhizome mass for any species studied. Only S. canadensis produced a greater number of rhizomes but lower biomass allocation to vegetative reproduction in habitats with bison. Each rhizome is a potential vegetative offspring (ramet), so producing a greater number of rhizomes could lead to faster vegetative spread if ramet recruitment rates are equivalent (or greater) in grazed habitats. Successful recruitment from seed in tallgrass prairie is rare and episodic (Benson and Hartnett, 2006), so vegetative reproduction is a very important mechanism of population growth and maintenance in prairie habitats regardless of habitats, and it might be expected to be particularly critical in habitats without bison where light- and space-limited conditions make the probability of successful recruitment from seed very low. If there is a trade-off between allocation to seed and vegetative reproduction, as has been proposed by some (Ronsheim and Bever, 2000; Sutherland et al., 1988; Thompson and Eckert, 2004; Worley and Harder, 1996), the increase in seed reproduction in bison-grazed habitats may have resulted in the lower allocation to vegetative reproduction observed in S. canadensis.
The lack of plasticity in vegetative reproduction despite other changes in growth could indicate vegetative reproduction may be more affected by species-specific constraints than by environment or changes in plant size. However, the phenology of rhizome bud production and outgrowth may differ relative to flowering and fruiting, and variation in rate of development could mean that this snapshot gave an incomplete picture of the true end-of-season rhizome production for some individuals. It is particularly important to improve our understanding of the factors regulating vegetative reproduction, particularly if trade-offs with sexual reproduction are involved, since for many perennial prairie species it is the primary mode of reproduction (Benson et al., 2004), and the relative numbers of recruits from seed vs. buds also strongly influences genetic diversity.
This study found the activities of bison increased growth and reproduction in all six forb species studied, though the species varied in strength and type of response. For Ambrosia psilostachya, Baptisia australis, Solidago canadensis, and Vernonia baldwinii, most measures of size and sexual reproduction were significantly greater in bison-grazed habitats while vegetative reproduction was not reduced in bison-grazed habitats. Plant size was not significantly different between habitats for A. ludoviciana and P. tenuiflorum, but at least one measure of sexual reproduction was significantly greater in prairie grazed by bison for those species. The removal of grass biomass by bison lessens the competitive ability of dominant grasses, decreases local neighborhood vegetation density, and increases the availability of light (and potentially other resources), leading to greater forb growth and reproduction.
BIOMASS ALLOCATION PATTERNS
Five out of six species showed significant differences in biomass allocation patterns between habitats, with the most prominent effect being decreased allocation to stem and increased allocation to seed reproduction in habitats with bison. Therefore, many species of perennial forbs are able to plastically alter their growth and biomass allocation strategies in response to environmental pressures. This is not surprising because tallgrass prairie is characterized by high spatial and temporal variability in the limitation and availability of different resources, which would be expected to select for high plasticity in biomass allocation. Only A. ludoviciana, which also showed little plasticity in size or reproduction, showed no significant differences in allocation to any function.
Since biomass allocation to leaves was not significantly different between habitats for all but one species, the reduction in stem allocation observed in four of the species studied was likely related to increased allocation to sexual reproduction. As might be expected for plants in very light-limited herbaceous communities, individuals of A. psilostachya in bison-absent habitats showed signs vertical growth was of enhanced importance, for stem allocation and height were both significantly greater, to the detriment of allocation to leaves and reproduction. In environments like the ungrazed habitat in this study where competition for light is intense, individuals may need to allocate a greater proportion of biomass to stem in order to maintain vertical growth towards greater light availability higher in the (taller) canopy and avoid death from insufficient light. In higher-light environments, vertical growth is less important, enabling the plant to invest some of the energy that would have been allocated to stem in reproduction. Therefore, for species that allocated biomass differently between the two habitats, there seemed to be a trade-off between allocation to stem and to sexual reproduction, which is consistent with light limitation promoting stem allocation more in bison-absent habitats than in bison-present habitats.
OTHER INDIRECT EFFECTS OF BISON
Though not the focus of this study, observed differences in plant phenology and insect damage between the two habitats appeared to contribute to some of the observed differences in plant performance. As none of the areas used in this study had been burned since the previous growing season, considerably more plant litter was present in the nongrazed habitats, which seemed to noticeably delay the growth and flowering of some species, particularly B. australis and V. baldwinii. Such differences in phenology could be caused by delayed soil warming due to the built-up biomass's blocking of sunlight, in addition to lower light resource availability slowing plant growth rate (Knapp and Seastedt, 1986). Delayed flowering proved to be particularly significant for B. australis since an outbreak of Epicauta sp. (blister beetles) a few weeks into the growing season consumed all flowers, flower buds, fruits below a certain size, and immature leaves. Outbreaks of Epicauta sp. herbivory are not an unusual occurrence for B. australis in tallgrass prairie (Evans, 1990). Since B. australis individuals in habitats with bison had few immature leaves and had bloomed earlier, the majority of their leaves and many fruits were left uneaten by Epicauta sp. However, due to the delay in phenology, individuals in ungrazed habitats had more immature leaves and no fruits too mature to be eaten by Epicauta sp., so all flowers and fruits and a significantly greater proportion of leaves were consumed by Epicauta sp. The observed difference in sexual reproduction between habitats for B. australis cannot be entirely attributed to the effects of insect herbivores, however, since significantly more flowers were produced in bison-grazed habitats and floral reproductive allocation was higher even when only rachis masses (rachises were uneaten by Epicauta sp.) were considered. Therefore, the differences in growth and reproduction between habitats for B. australis were magnified by a combination of insect herbivory and differences in phenology.
Individuals of V. baldxoinii in habitats with bison matured and began to develop flowers earlier than individuals in ungrazed habitats. Since any V. baldwinii floral buds that had not opened before a certain warm dry period in July failed to mature any further in either habitat, no seeds or mature flowers were produced by individuals in habitats without bison due to their delayed phenology.
Tallgrass prairies are complex ecosystems characterized by a complex network of interactions between species within and among trophic levels. The presence of large grazers has been shown to have a significant impact on other types of organism within the tallgrass prairie (Joern, 2005; Moran, 2014; Powell, 2006), so it is not surprising that some of the effects of bison observed in this study were mediated by interactions with other organisms. Many other studies have found plant responses to the common major disturbances of fire and grazing in tallgrass prairie are often mediated indirectly by other biotic interactions (Hajny et al., 2011; Wilson et al., 2001) or by weather conditions (Fahnestock and Knapp, 1994; Fay et al., 2003; La Pierre et al., 2011).
In summary, this study found evidence the activities of large grazers in tallgrass prairie increase available light, reduce grass canopy height and density, and therefore reduce the intensity of inter-specific plant competition. The results support the hypothesis that release from competition with grasses contributes to the increased growth, reproduction, abundance, and species richness of forbs in tallgrass prairie habitats with bison. The results further indicate perennial forbs in tallgrass prairie show high phenotypic plasticity in life history traits such as growth, reproduction, and resource allocation patterns in response to the spatio-temporal heterogeneity in resources generated by large vertebrate grazers and other drivers. Since the preservation of the floristic diversity of the highly endangered tallgrass prairie ecosystem is an important conservation issue, it is critical that we continue to increase our understanding of how management decisions like grazing lead to changes in species populations.
Acknowledgments.--This project was supported by the Konza Prairie Long-Term Ecological Research program (NSF DEB-1440484), The Konza Prairie Biological Station, the Kansas State University Division of Biology, the Kansas Native Plant Society, and the Grassland Heritage Fund. Two anonymous reviews provided many suggestions that greatly improved the manuscript.
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Submitted: 26 September 2016
Accepted 11 July 2017
ANNA ELSON and DAVID C. HARTNETT (1)
Division of Biology, Kansas Slate University, Manhattan, Kansas 66506
(1) Corresponding author: e-mail: firstname.lastname@example.org
Caption: Fig. 1.--(a) Mean ([+ or -] 1 SE) proportional canopy cover of neighboring grass, forbs, shrubs, and of bare ground (within a 0.5-m radius) of sampled perennial forb individuals in tallgrass prairie habitats with and without the presence of bison. Asterisks indicate a significant difference between habitats al the P [less than or equal to] 0.05 level, (b) Mean ([+ or -] 1 se) vegetation density (g/[m.sup.2], as measured by settling height of a pasture disk) in prairie habilats with and without bison. Asterisks indicate a significant difference between habitats at the P [less than or equal to] 0.05 level, (c) Mean ([+ or -] 1 SE) percentage of ambient photosynthetically active radiation ([micro]mol x [m.sup.-2] x [s.sup.-1]) at different positions within the plant canopy in tallgrass prairie habitats with and without bison. Asterisks indicate a significant difference between habitats at the P [less than or equal to] 0.05 level, (d) Mean ([+ or -] 1 SE) species richness per transect of nongraminoid species found within a 0.5-m radius of sampled individuals in tallgrass prairie habitats with and without bison. Asterisks indicate a significant difference between habitats al the P [less than or equal to] 0.05 level
Caption: Fig. 2.--The mean percentage ([+ or -] 1 SE) of total aboveground biomass in stems, leaves, and reproductive structures in six perennial forb species in tallgrass prairie habitats with and without the presence of bison. Asterisks indicate a significant difference between habitats at the P [less than or equal to] 0.05 level
Table: 1.--Mean ([+ or -] 1 SE) measures of growth (aboveground biomass, height, and number of leaves produced) and reproduction (inflorescence biomass, number of reproductive structures, percentage of individuals flowering) for six perennial forbs in tallgrass prairie habitats with and without the presence of bison Species Habitat Above-ground biomass Ambrosia psiloslachya With bison 1.616 [+ or -] 0.233 Without bison 0.940 [+ or -] 0.244 prob. 0.049 Artemisia ludoviciana With bison 1.550 [+ or -] 0.162 Without bison 1.182 [+ or -] 0.167 prob. 0.119 Baptisia australis With bison 53.342 [+ or -] 5.419 Without bison 11.760 [+ or -] 5.241 prob. <0.0001 Psoralidium terniflorum With bison 24.254 [+ or -] 4.202 Without bison 19.792 [+ or -] 4.132 prob. 0.452 Solidago canadensis With bison 9.142 [+ or -] 0.892 Without bison 4.827 [+ or -] 0.879 prob. 0.001 Vernonia baldwinii With bison 8.812 [+ or -] 0.782 Without bison 3.435 [+ or -] 0.782 prob. <0.0001 Species Height (cm) Number of leaves * Ambrosia psiloslachya 38.80 [+ or -] 1.63 85.31 [+ or -] 10.28 44.38 [+ or -] 1.71 65.75 [+ or -] 10.75 0.021 0.193 Artemisia ludoviciana 36.71 [+ or -] 1.97 301.31 [+ or -] 45.57 37.58[+ or -] 2.02 227.36 [+ or -] 46.94 0.761 0.262 Baptisia australis 35.97 [+ or -] 1.34 600.17 [+ or -] 56.40 24.81 [+ or -] 1.30 219.65 [+ or -] 54.55 <0.0001 <0.0001 Psoralidium terniflorum 51.83 [+ or -] 2.38 2129.0 [+ or -] 490.2 58.50 [+ or -] 2.38 1902.1 [+ or -] 490.2 0.053 0.745 Solidago canadensis 73.70 [+ or -] 3.44 141.72 [+ or -] 13.92 67.58 [+ or -] 3.39 94.45 [+ or -] 13.71 0.209 0.018 Vernonia baldwinii 50.80 [+ or -] 2.89 56.93 [+ or -] 3.75 44.95 [+ or -] 2.89 35.37 [+ or -] 3.75 0.158 0.0001 Species Reproductive biomass (g) ** Ambrosia psiloslachya 0.235 [+ or -] 0.042 0.084 [+ or -] 0.044 0.017 Artemisia ludoviciana 0.168 [+ or -] 0.034 0.088 [+ or -] 0.035 0.102 Baptisia australis 1.798 [+ or -] 0.2443 0.069 [+ or -] 0.236 <0.0001 Psoralidium terniflorum 4.102 [+ or -] 0.736 1.604 [+ or -] 0.736 0.019 Solidago canadensis 1.610 [+ or -] 0.209 0.349 [+ or -] 0.205 <0.0001 Vernonia baldwinii 1.373 [+ or -] 0.212 0.007 [+ or -] 0.212 <0.0001 Species Number of reproductive structures*** Ambrosia psiloslachya 42.229 [+ or -] 7.366 22.406 [+ or -] 7.703 0.067 Artemisia ludoviciana 210.57 [+ or -] 39.38 105.73 [+ or -] 40.56 0.068 Baptisia australis 46.79 [+ or -] 3.96 5.42 [+ or -] 3.83 <.001 Psoralidium terniflorum 180.60 [+ or -] 46.51 100.87 [+ or -] 46.51 0.230 Solidago canadensis Not measured Vernonia baldwinii 68.367 [+ or -] 8.370 2.333 [+ or -] 8.370 <0.0001 Species Percent (lowering Ambrosia psiloslachya 97.1 [+ or -] 2.8 81.4 [+ or -] 7.0 0.069 Artemisia ludoviciana 65.7 [+ or -] 8.0 39.4 [+ or -] 8.5 0.035 Baptisia australis 86.2 [+ or -] 6.4 29.0 [+ or -] 8.2 0.0001 Psoralidium terniflorum 93.3 [+ or -] 4.6 86.7 [+ or -] 6.2 0.401 Solidago canadensis 87.5 [+ or -] 5.8 51.5 [+ or -] 8.7 0.004 Vernonia baldwinii 80.0 [+ or -] 7.3 16.7 [+ or -] 6.8 <0.0001 * Total number of leaf nodes for all species except A. ludoviciana, for which it indicates the total number of living leaves present. ** For B. australis, only the mass of rachis(es) was included. *** Number of female flowers for A. psiloslachya, number of flowers for A. ludoviciana and V. baldxoinii, floral nodes for B. australis, and fruits for P, tenuiflorum. No data available for S. canadensis because counting of flowers was impractical. Table 2.--Measures of vegetative reproduction (mean biomass allocation to rhizomes, and mean number of rhizomes per ramet) for three clonal tallgrass prairie perennials in habitats with and without the presence of bison Species Habitat Vegetative reproductive allocation * Baptisia australis With bison 0.00479 [+ or -] 0.00122 Without bison 0.00736 [+ or -] 0.00167 prob. 0.089 Solidago canadensis With bison 0.204 [+ or -] 0.024 Without bison 0.294 [+ or -] 0.028 prob. 0.016 Vernonia baldwinii With bison 0.00632 [+ or -] 0.001 Without bison 0.0091 [+ or -] 0.001 prob. 0.059 Species Number of rhizomes Baptisia australis 5.96 [+ or -] 0.74 3.48 [+ or -] 0.72 0.02 Solidago canadensis 16.06 [+ or -] 2.07 17.24 [+ or -] 2.03 0.68 Vernonia baldwinii 11.1 [+ or -] 0.72 6.8 [+ or -] 0.72 <0.0001 * Calculated as the ratio of rhizome mass (g) to total aboveground plant mass (g).
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|Author:||Elson, Anna; Hartnett, David C.|
|Publication:||The American Midland Naturalist|
|Date:||Oct 1, 2017|
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