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Prescribed burning and understory composition in a temperate deciduous forest, Ohio, USA
Forest Ecology and Management 238 (2007) 54–64 www.elsevier.com/locate/foreco
Prescribed burning and understory composition in a temperate deciduous forest, Ohio, USA Lance S. Glasgow, Glenn R. Matlack * Environmental and Plant Biology, Porter Hall, Ohio University, Athens, OH 45701, USA Received 24 June 2006; received in revised form 30 August 2006; accepted 30 August 2006
Abstract Since the advent of widespread suppression in the mid-20th century, fire has been relatively rare in deciduous forests of the eastern United States. However, widespread prescribed burning has recently been proposed as a management tool to favor oak (Quercus spp.) regeneration. To examine the potential effects of fire introduction on the understory community, we experimentally burned small plots and simulated aspects of fire at a forested site in southeastern Ohio. Treatments included two burn intensities, litter removal, increased soil pH, and a control. Treatments were arranged in a randomized block design in two landscape positions (dry upland and moist lowland) and two canopy conditions (gap, no gap). Postfire vegetation was identified to species, and stems were counted 1, 3, and 14 months after burning. Community composition was more strongly affected by fire in upland plots than in lowlands, but was not affected by canopy openness. Both cool and hot burns reduced post-fire seedling emergence of Acer rubrum, a common overstory tree. Hot burns facilitated germination of Vitis spp., Rhus glabra, and Phytolacca americana, species common in disturbed habitats, and increased graminoid abundance. Cool burns and litter removal facilitated germination of Erechtites hieracifolia and Liriodendron tulipifera suggesting that litter removal is the mechanism by which fire favors colonization. These results suggest that fire applied frequently in the Central Hardwoods Region would cause compositional shifts to graminoids and disturbance-adapted forbs by increasing germination from the seed bank. Fire did not favor species with dormant underground buds, as studies in other ecosystems would suggest. Vegetational responses were noticeably weaker in the second year after burning, indicating that a single fire has only a short-term effect. # 2006 Elsevier B.V. All rights reserved. Keywords: Forest herbs; Prescribed fire; Central Hardwoods Region
1. Introduction If fire is introduced to a long-unburned Central Hardwoods forest for management purposes, what will the consequences be for the native flora? If fire has been historically common in the region, as some studies suggest, we can expect the present flora to consist of species which tolerate regular burning. In fact, many Central Hardwoods species have growth forms and life histories which appear to pre-adapt them to tolerate fire. The history of fire in the region is not clear, however, and it is difficult to predict the fire responses of herb and shrub species based on life history, alone. If fire management is based on a misunderstanding of plant life history, or on an incorrect reading of the historical record, burning could potentially have large effects on forest community diversity. Thus, there is a need to assess the community-level implications of prescribed
* Corresponding author. Tel.: +1 740 593 1131; fax: +1 740 593 1130. E-mail address: [email protected] (G.R. Matlack). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2006.08.344
burning in Central Hardwoods forests. The question has some urgency because widespread prescribed burning has been proposed as a management tool to encourage oak regeneration (Abrams, 1992; Sutherland et al., 2003a). The fire history of the Central Hardwoods Region (CHR) is poorly understood. Today, fire rarely occurs in deciduous forests of the CHR (Yaussy and Sutherland, 1994; Lafon et al., 2005), but fire scar records show that some oak-dominated stands burned regularly in the late 19th and early 20th centuries (Sutherland, 1997; Shumway et al., 2001; Guyette and Spetich, 2003; Soucy et al., 2005; McEwan, 2006). Mean return times were as little as 5.4 years in some sites. Clearly fire has been a frequent event in some parts of the landscape, but it is difficult to generalize to the region as a whole or to a broader time scale. It is possible that natural ignition only occurs on a scale of centuries in some areas, and that much of today’s forest flora has not evolved to tolerate fire. Consistent with a low fire frequency, the modern flora does not show adaptations commonly associated with fire such as serotiny, epicormic sprouting, or a germination requirement for bare mineral soil. It
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is unclear how a flora lacking such adaptations would respond to the introduction of fire. 1.1. Fire in today’s forest Fires in the modern CHR forest tend to be of low intensity with flame lengths rarely greater than 1 m in height, and are usually confined to surface fuels (Elliott et al., 1999; Iverson and Hutchinson, 2002). Such fires typically remove a portion of the leaf litter and increase calcium available in the soil (Boerner et al., 2003; Hutchinson et al., 2005). Herb species richness, diversity, and cover have been shown to increase following fire in the region (Nuzzo et al., 1996; Arthur et al., 1998; Hutchinson and Sutherland, 2000; Kuddes-Fischer and Arthur, 2002). In Appalachian mixed-oak forests, increases in herbaceous richness and cover have been correlated with a decrease in woody plant cover, suggesting a response to light (Elliott et al., 1999; Kuddes-Fischer and Arthur, 2002; Vandermast et al., 2004). Post-fire increases in species diversity have usually been small, however, and compositional changes typically last no more than 1–2 years (Nuzzo et al., 1996). Although little is known about the fire responses of individual herb and shrub species in the region, it is possible to predict responses based on growth form and life history. The CHR herb layer is dominated by perennial species sprouting annually from buried tubers or rhizomes (Bierzychudek, 1982; Whigham, 2004). Many shrubs have the capacity to regrow from rhizomes or root crowns. In fire-prone ecosystems, shrub and perennial herb species often rely on soil-protected buds to resprout quickly following fire (Platt et al., 1988; Matlack et al., 1993a,b). Buds have been observed to initiate growth in response to a fire’s heat (Flinn and Pringle, 1983), mortality of apical meristems (Matlack, 1997), or exposure of bare soil (Platt et al., 1988). Although the dormant below-ground buds of many CHR species have not necessarily evolved in response to fire, possession of protected buds may allow them to reestablish quickly after fire. Sprouting capacity may pre-adapt many herb and shrub species to survive prescribed fires with little negative effect. 1.2. Seed germination In fire-prone ecosystems, fire is often followed by a flush of germination from the seed bank (Lemon, 1949; Keeley et al., 2003; Milberg and Lamont, 1995; Morgan, 2001). Seed banks in deciduous forest sites are generally small relative to those of other North American ecosystems (Harper, 1977), and typically include disturbance-oriented annual and perennial herb species (Matlack and Good, 1990; Hyatt and Casper, 2000; Schelling, 2006). Fire appears to have the potential to cue germination in some of these species. In mixed hardwood forest of southeast Ohio, several species have been observed to colonize burned sites by germination from seed, including Rubus spp., Rhus glabra, Vitis spp., Phytolacca americana, Erechtites hieracifolia, Carex spp., Panicum spp., and Eupatorium rugosum (Hutchinson and Sutherland, 2000; Vandermast et al., 2004; Hutchinson et al., 2005). These species are normally found in
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forest edges, treefall gaps, and other non-fire disturbances, suggesting that fire may encourage them through its impact on canopy openness and soil disturbance. We predict that prescribed burning would cause a compositional shift to such species by promoting seedling recruitment. Removal of live and dead vegetation often triggers germination in fire-prone communities. In Florida oak scrub, for example, the colonization dynamics of understory species are largely controlled by fire-formed gaps in the dominant shrub layer; several endemic species are only found in these gaps (Menges and Hawkes, 1998). Mechanical removal of vegetation or litter has been shown to produce vegetational effects similar to fire in such communities (Greenberg et al., 1995; McConnell and Menges, 2002). In the absence of fire, vegetation and litter often inhibit germination by preventing seed contact with soil and blocking light necessary for germination (Klinkhammer and Jong, 1988; Fowler, 1988; Xiong and Nilsson, 1999; McConnell and Menges, 2002; Vickery, 2002). Presumably, fire would act on vegetation in the CHR by removing litter and vegetational inhibition, thereby promoting recruitment. Seedling germination and survival might be further enhanced by release of nutrients following fire (Romanya et al., 1994). We report a small-plot experiment designed to test the fire effects postulated above. Natural vegetation in a CHR forest site was subjected to fire and two fire surrogate treatments. The small size of individual plots allowed a high degree of control over the intensity and uniformity of treatments, and allowed a precise spatial linkage of treatments and vegetation response. Interactions were examined between treatments and landscape position and canopy openness, two important non-fire factors shaping vegetation in this community. Because understory species may vary widely in their responses to fire, we considered species responses individually. Based on observations in other plant communities (above), we hypothesized that fire in a CHR site would favor seedbank species and species able to propagate from protected meristems. We expected fire to control germination through litter removal, reasoning that litter accumulation would impede seedling establishment (Xiong and Nilsson, 1999; McConnell and Menges, 2002; Vickery, 2002). Germination is also known to respond to heat and smoke in some cases (Brown and van Staden, 1997; Bellairs et al., 2006). Because all of these effects are dependent on fire exposure, the effects of fire were expected be greater in more intense burns, and to vary with landscape position and canopy openness to the extent that these factors influence local fire intensity. 2. Methods 2.1. Study area Experimental plots were established in the Vinton Furnace Experimental Forest (VFEF) (398110 N, 828220 W) on the unglaciated Alleghany Plateau of southeastern Ohio, USA. The study area is adjacent to the Ohio Hills site of the US Forest Service’s Fire and Fire Surrogate experiment (Iverson et al., 2004), and our treatments were designed to mimic treatments in
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that study. The area is dissected by narrow ridges and small valleys with elevations ranging from 200 to 300 m a.s.l (Brockman, 1998). Soils are moderately to well-drained sandy and silt loams derived from sandstone, siltstone, and shale (Lemaster, 2004). Southeastern Ohio has a humid-continental climate, with an average annual temperature of 11.3 8C and annual precipitation of 1024 mm (NOAA, 2004). Natural vegetation is a mixed deciduous forest characteristic of the Low Hills section of the Allegheny Plateau (Braun, 1950). Valley sites are relatively moist with canopies dominated by Acer saccharum, Nyssa sylvatica and Liriodendron tulipifera. Ridges and south-facing slopes are drier and dominated by Quercus spp., Carya spp., and A. rubrum. Understory community composition is largely determined by topographic position (Small and McCarthy, 2002) and canopy openness (Hughes and Fahey, 1991; Reader and Bricker, 1992). All sites used in this study were cleared for fuelwood in the 19th century, but were not cultivated. Sites are now covered with long-established second growth forest. The ground flora is generally species-rich with a well-developed herbaceous community. Surveys of fire scars show that two nearby stands burned often between ca. 1870 and 1930, but that fire was usually limited to dry ridges and upper slope positions (Sutherland, 1997; Hutchinson and Sutherland, unpublished). Those fires were probably anthropogenic in origin (Yaussy and Sutherland, 1994). There is no record of fire at the sites used in the present study, and the study area has been fire-free for several decades at least. Experimental plots were established in apparently homogeneous, level microsites which included no plant stems >1 cm diameter. A comparison with randomly chosen microsites in adjacent forest (Glasgow and Matlack, 2007) found no significant difference in any of fifteen edaphic and vegetational variables, suggesting that the experimental sites were typical of forest in their respective landscape positions. Herbaceous species were dormant when plots were established in December 2003, so the richness and stem density of individual plots was not known beforehand. Occasional woody stems were clipped at ground level. 2.2. Treatments Treatments were applied in five 2 m 2 m permanent plots at each site. To asses the effects of prescribed fires on establishment of understory vegetation, plots in the cool burn treatment were burned using only the pre-existing leaf litter as fuel. A fine mist of kerosene was sprayed on the fuel beforehand to ensure uniform ignition. Temperatures in burn treatments were monitored with pyrometer tags marked with temperaturesensitive paint (Glasgow and Matlack, 2007). Temperatures at the soil surface ranged from 84 to 195 8C, with flame lengths of 5–15 cm. Prescribed burns in deciduous forest tend to be patchy, varying in intensity according to local fuel loading, moisture, and slope (Gibson and Good, 1987; Franklin et al., 1997), and some microsites within the fire perimeter experience temperatures much higher than the average value. To simulate the effects of hotter burns on the understory flora, we increased
fuel loading by adding twenty air-dry pine furring strips (3 cm 3 cm 200 cm) in the hot burn treatment. Pine strips were evenly spaced on top of the existing leaf litter. Paint tags in the hot burns consistently reached 150–230 8C hotter than those in cool burns. These temperatures are comparable to average and extreme values recorded in prescribed burns in the study area (Iverson and Hutchinson, 2002). Flame lengths varied from 10 to 30 cm. To test litter removal as a mechanism by which fire effects understory plant recruitment, leaf litter was removed by hand down to the humic layer simulating the effect of a ground-level fire (litter removal treatment). Caution was used not to disturb the humic soil surface. In the fourth treatment, agricultural lime was added to simulate nutrient addition from ash (lime addition). In deciduous forests of southeastern Ohio, the most significant change in soil chemistry following fire is an increase in calcium and elevation in soil pH (increasing from ca. 3.8 to 4.2 units; Boerner et al., 2003, Boerner, personal communication). Lime was added as needed to contribute Ca and to raise the pH in each plot 0.4 units (Glasgow and Matlack, 2007). Finally, a control treatment with no manipulation was also established. Treatments were applied between April 5th and April 9th, 2004, to coincide with burn treatments in the nearby Fire and Fire Surrogate study (Iverson et al., 2004). 2.3. Experimental design A factorial design was used to test the effects of fire, canopy openness, and landscape position on understory vegetation. The five experimental treatments were applied in each of 20 sites in a forested area of ca. 2000 ha. All sites were situated at least 50 m from roads and other large openings to avoid edge effects (Matlack, 1993, 1994), and at least 250 m from other sites to ensure statistical independence. To test how canopy openness and landscape position interact with fire, sites were established in two landscape positions (ridge tops and valleys) and in two canopy conditions (open and closed). Valley plots were located on terraces beside small streams. Open-canopy sites were selected in natural canopy openings. Small trees and saplings were felled as needed to ensure a minimum canopy openness of 40% measured at a central point. Each landscape position canopy-openness combination was replicated five times, giving a total of 100 plots in twenty sites. Landscape canopy combinations were evenly distributed across the study area. All vascular plants emerging after treatment were identified to species following Gleason and Cronquist (1991). Stem number was recorded by species in July and September 2004 to quantify mid- and late-summer response, respectively, and in June 2005 to test vegetation response one year following fire. In each plot, all data were collected in a centered 1 m2 sub-plot to avoid variation at plot edges. 2.4. Analysis Nonmetric multidimensional scaling (NMS) was used to assess trends in species composition at all sample dates (PCORD, MJM Software, Gleneden Beach, Oregon). NMS is a
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non-parametric iterative ordination technique well suited for non-normal data sets typical of ecological studies (McCune and Grace, 2002). NMS uses ranked distances to ordinate experimental plots in species space along a series of axes determined by a minimum stress configuration (a measure of departure from monotonicity). NMS was run on data from each sample date using Bray–Curtis distance measures, four axes, 200 iterations, and an instability criterion of 0.0001. A Monte Carlo test was used to determine the minimum number of dimensions required to yield the lowest stress. A threedimensional solution was deemed appropriate for all data sets. A randomized complete block ANOVA was performed on species richness, Shannon–Weiner diversity (H0 ), and total stem number in each plot. Canopy openness, landscape position, and treatment were included as main effects. Species correlated with NMS axis scores (r > 0.45) were reanalyzed individually within the respective landscape positions to detect individual responses to treatments and canopy openness. ANOVA of stem number was followed by a Tukey–Kramer multiple comparison test to determine significant differences among treatments. 3. Results A total of 72 forbs, 6 ferns, 35 woody species, and 7 graminoids were identified in experimental plots between July 2004 and June 2005 (Appendix A). Stem density and species frequency across all plots were dominated by three taxa: A. rubrum, L. tulipifera, and Rubus spp. Smilax rotundifolia, Carex sp. 1, and Desmodium nudiflorum were widely present at low levels, but showed high densities in individual ridge plots. Likewise, high densities of Pilea pumila, Deparia acrostichoides, and Panicum commutatum were recorded in several
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valley plots. Species richness and total stem density were significantly greater in valleys than on ridges for all sample dates (Fig. 1). Species diversity (H0 ; not shown) showed the same pattern of significance as richness ( p < 0.05). Stem density was significantly greater in canopy openings than under closed canopies in September 2004 and June 2005. Richness was significantly greater under closed canopies than in gaps in July 2004 but the difference decreased at later dates and was not statistically significant (Fig. 1). Diversity was not significantly affected by canopy openness. Fire and fire surrogate treatments had little effect on total stem density, species richness, or diversity (ANOVA, P > 0.05). 3.1. Species composition Landscape position separated plots along the first NMS axis in July 2004 (33.2% of variation) and September 2004 (Fig. 2; 30.8% of variation) and along axis 2 in June 2005 (31.4% of variation). In each case, the axis most clearly separating landscape positions explained the greatest variation in the analysis. Most of the species which correlated strongly with axis 1 in July 2004 and axis 2 in June 2005 were understory herbs typical of valleys (Table 1). In September 2004, woody species were also strongly correlated with the ridge-valley axis: R. glabra was primarily found in valleys, while A. rubrum and Sassafras albidum were associated with ridges. Because ridge and valley communities differed markedly in composition, plots in the two communities were re-analyzed separately to test for compositional effects of canopy openness. NMS showed separation between open and closed canopies within both ridge and valley sites in September 2004 (Fig. 3), but canopy types were more clearly separated on ridges. In
Fig. 1. Comparisons of stem density and species richness between landscape positions and canopy openness. Error bars represent the standard error. An asterisk (*) indicates a significant difference in overall ANOVA between valleys and ridges or open and closed canopies. Significance: *P < 0.05; **P < 0.01; ***P < 0.001.
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(r = 0.49) was predominantly found in gaps. Canopy openness effects were less apparent in July 2004 and June 2005. 3.2. Fire and fire surrogate treatments
Fig. 2. Ordination of plots by species in nonmetric multidimensional scaling (NMS), September 2004. Axis 1 accounts for 30.8% of the of the total variation explained by the analysis. The convex polygons encompass all Ridge and Valley sites, respectively. The ellipse indicates an outlying Ridge site. Ordinations from all other sample dates show similar degrees of clustering. Codes: ‘‘c’’ as a first letter, closed canopy; ‘‘o’’, open canopy; ‘‘c’’ as a second letter, control; ‘‘cb’’ as second and third letters, cool burn; ‘‘hb’’, hot burn; ‘‘l’’, litter removal; ‘‘f’’, lime addition.
valley communities in September 2004, plots were separated by canopy openness along axis 1 (20.6% of variation; Fig. 3a). The understory herbs Asarum canadense (r = 0.52), Galium triflorum (r = 0.62), Potentilla sp. 1 (r = 0.501), and Potentilla simplex (r = 0.51) were negatively correlated with scores on the first axis indicating abundance under closed canopies, while the woody species A. rubrum (r = 0.51), and L. tulipifera (r = 0.55) were positively correlated, indicating presence in canopy gaps. In ridge communities plots were separated by canopy openness on axis 3 (33.0% of variation) (Fig. 3b). D. nudiflorum (r = 0.59) and R. glabra (r = 0.48) were strongly associated with low values on the third axis indicating preference for a closed canopy, while Pinus sp. Table 1 Pearson product-moment correlations (r > 0.45) of species abundance with scores on NMS axes which most strongly separated plots by landscape position Taxa Acer rubrum Cimicifuga racemosa Circaea lutetiana Cardamine concatenata Galium triflorum Pilea pumila Potentilla sp. 1 Rhus glabra Sassafras albidum Viola sororia
July 2004, axis 1
September 2004, axis 1
June 2005, axis 2
0.497 0.508 0.523 0.513 0.617 0.518
0.649
0.754 0.490 0.530 0.465 0.688
Positive correlation coefficients indicate higher densities in valleys.
Because there is a strong a priori reason to expect a separation of species composition by landscape position, and such an effect is demonstrated above, compositional effects of fire and fire surrogate treatments were examined separately for ridge and valley sites. In ridge communities, plots were clearly separated by treatments along axis 2 in July 2004 (40.2% of variation) and axis 1 in September 2004 (21.1% of variation) (Fig. 4). Hot burn plots on ridges tended to be dominated by graminoids in both density and frequency, including Carex sp. 1 (likely C. wildenovii), P. commutatum and Panicum sp. 1 (likely P. dichotomum), arising as both seedlings and vegetative shoots. Woody species were also frequently observed in hot burns, including L. tulipifera, Rubus spp., R. glabra and Vitis spp.. Abundance of R. glabra, Carex sp. 1, P. americana, L. tulipifera, and Rubus spp. on ridges showed positive correlations with scores on axes separating treatments (Table 2), suggesting these species were favored by fire. A. rubrum showed a negative correlation with axes in July and September, respectively, suggesting that abundance of this species declines with fire. Separation between treatments was less distinct in September 2004 than in July, and was no longer apparent in 2005, indicating that the effects of fire on ridge community composition persisted less than a year. Species that showed moderate to strong correlations (r > 0.45) with NMS axes were analyzed by ANOVA within landscape positions, with canopy openness and treatment as main effects. Canopy openness was not significantly related to frequency in any of the species date landscape position combinations examined, thus, only F-values for the treatment term are reported. In ridge communities in July, stem number of A. rubrum was significantly greater in non-burn treatments than in burn treatments (F = 4.80, d.f. = 4, P < 0.01; Tukey–Kramer multiple comparison test P < 0.05). Stem number of R. glabra was significantly greater in the hot-burn treatment than in all other treatments (F = 7.93, d.f. = 4, P < 0.001; Tukey–Kramer P < 0.05), suggesting that fire intensity is critical to recruitment in this species. L. tulipifera seedlings were significantly more abundant in cool burn treatments than in the control, lime addition, or hot burn treatments (F = 10.43, d.f. = 4, P < 0.0001; Tukey–Kramer P < 0.05), but cool burns were not distinguishable from the leaf litter treatment, implying that fire acts on Liriodendron recruitment by removal of leaf litter. Presence of cotyledons on most individuals of these species indicates that regeneration was primarily caused by germination. In September 2004 no taxa were significantly affected by treatments or canopy openness on ridges (ANOVA, P 0.05). In valley communities separation among treatments was not as distinct as on ridges, only appearing in July 2004 (24.5% of variation, axis 3, not shown). In the ordination, hot burns were distinct from non-burn treatments, and cool burns were transitional between hot burns and all other treatments. P. americana showed a strong positive correlation with axis 3 in
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Fig. 3. Ordination of plots in (a) valleys and (b) ridge-top sites according to total species composition in September 2004 by nonmetric multidimensional scaling (NMS). Convex polygons include all gap and no gap sites, respectively. Circles represent outliers in the open and closed canopy data in the valley community. Codes: ‘‘c’’, control; ‘‘cb’’, cool burn; ‘‘hb’’, hot burn; ‘‘l’’, litter removal; ‘‘f’’, lime addition.
valley communities (Table 2), indicating that this species increased following fire. As in ridge communities, A. rubrum showed strong negative correlation with axis 3, again suggesting that fire inhibits germination or seedling survival. When analyzed individually, stem number of A. rubrum in valleys was found to be significantly greater in control plots than in lime addition, cool burn or hot burn treatments (F = 7.17, d.f. = 4, P < 0.001; Tukey–Kramer P < 0.05). A significantly greater number of P. americana seedlings were observed in hot burns than in other treatments, suggesting that germination of P. americana in valleys is controlled by fire intensity (F = 5.38, d.f. = 4, P < 0.01; Tukey–Kramer P < 0.05). Neither A. rubrum nor P. americana responded to canopy openness in valleys (ANOVA, P > 0.05). The responses of Vaccinium pallidum, E. hieracifolia, and Vitis spp. to fire were examined individually because these species have been shown to respond positively in other studies in the region (Elliott et al., 1999; Hutchinson and Sutherland, 2000). Landscape position, canopy openness, and treatment were included as main effects. E. hieracifolia was significantly influenced by treatments in July 2004 (ANOVA, Table 2 Correlations of species abundance with scores on NMS axes which most strongly (r > 0.45) separated plots by experimental treatment Taxa Rhus glabra Carex sp. 1 Phytolacca americanaa Liriodendron tulipifera b Rubus spp. Acer rubrum Acer rubruma
July 2004, axis 2
September 2004, axis 1
0.722 0.621 0.483 0.563 0.533 0.721 0.772
0.722
Positive correlations indicate higher densities in burned plots. Ridge and valley data are considered separately. a Distributions in valley sites; the remainder describe ridge communities. No correlations of r > 0.45 were recorded in June 2005. b Measured in August 2004.
F treatment = 15.05, d.f. = 4, P < 0.0001). Stem number was significantly higher in cool burn treatments than in hot burns, lime addition, or control treatments; and significantly greater in litter removal treatments than in control and lime addition treatments (Tukey–Kramer P < 0.05). Stem number of Vitis spp. was significantly higher in hot burns than in control, lime addition and leaf litter removal treatments (F treatment = 3.55, d.f. = 4, P < 0.05; Tukey–Kramer P < 0.05) and greater in uplands than valleys (F landscape = 7.09, d.f. = 1, P < 0.01). Almost all Vitis individuals were seedlings, as indicated by presence of cotyledons, implying that hot burns facilitate germination of this species. ANOVA detected no significant differences in stem density for V. pallidum. Neither Vitis spp., E. hieracifolia, nor V. pallidum responded to canopy openness (ANOVA, P > 0.05). Data recorded in the June 2005 were not analyzed because NMS failed to show separation among treatments. 4. Discussion Landscape position and canopy gaps are major factors structuring vegetation in deciduous forests of the eastern United States (Hughes and Fahey, 1991; Reader and Bricker, 1992; Olivero and Hix, 1998; Small and McCarthy, 2002) and they were important in our sites. Valley plots contained more stems and more species than ridge plots and were largely distinct in understory composition, a contrast which created a twocommunity background for the fire treatments. Canopy openness led to greater collective stem density, lower richness at some dates, and abundance of some individual species, although many widely recognized gap-occupying species showed no response. Failure to respond suggests that the openings used here were too small to substantially change the forest microclimate. Experimental burning caused changes in understory composition, effects most clearly evident in the ridge sites. Fire effects were evident despite considerable patchiness in the herb flora and the potential interaction of patchiness with small plot size. Many stems were observed in
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Fig. 4. Ordinations of ridge-top sites showing separation among treatments. Convex polygons each enclose all sites in a particular treatment. Circles indicate outliers in the hot and cool burn clusters. Ordinations are not shown for the 2005 data sets because NMS did not distinguish compositional differences between treatments. Codes: ‘‘o’’, open canopy; ‘‘c’’, closed canopy.
most experimental plots. Species recorded in plots included most of those growing in the immediate area, and many of the most common forest herb and shrub species in the region. Thus, we assume these results offer a fair description of the potential impact of fire in this forest community. 4.1. Life histories of fire responders Four types of fire response can be recognized among the species examined here. Emergence of shoots was either inhibited by fire, facilitated by hot fires, facilitated by cool fires and removal of leaf litter, or apparently unaffected. Addition of lime did not appear to influence emergence of forest species. We conclude that fire-caused changes in pH and Ca are not related to the vegetational effects reported here. Three taxa, R. glabra, Vitis spp., and P. americana, illustrate the response to fire intensity, with germination facilitated by hot burns but showing little response to cool burns or litter removal. Germination of each species was consistent with post-fire performance in other studies in CHR forests (DeSelm and Clebsch, 1991; Hutchinson and Sutherland, 2000; Vandermast et al., 2004). More commonly, all three taxa regularly establish in open sites in the absence of fire (Luken et al., 1997; Hyatt and Casper, 2000), demonstrating that germination can also be caused by non-fire disturbance. Germination of R. glabra has been shown to increase when seeds are warmed (Shelton and Cain, 2003) possibly reflecting adaptation to solar warming as a germination cue. Vitis spp. can germinate in canopy openings in which litter and soil are not disturbed (Haywood, 1994; Luken et al., 1997), again consistent with solar warming. Thus, the response to high-intensity fire appears to parallel a non-fire response to canopy disturbance. Sensitivity to soil warmth, a useful gauge of canopy openness in non-fire disturbances, may function as a pre-adaptation to fire intensity in burned sites. Other species responded primarily to cool fires. L. tulipifera, a common gap-occupying canopy tree (Clinton et al., 1994), showed high germination rates in both cool burn and litter-
removal treatments, suggesting that the two treatments are equivalent for the establishment of this species. Removal of leaf litter is known to be a mechanism by which fire alters community composition in other ecosystems, presumably by providing favorable microsites for seed germination (Greenberg et al., 1995; McConnell and Menges, 2002). L. tulipifera does not have any obvious adaptations to fire, however, and is largely absent from fire-shaped ecosystems of North America (Prasad and Iverson, 2006), implying a lack of evolutionary experience with fire. In this study hot burns led to decreased germination, again consistent with non-adaptation to fire, so the cool fire response observed here is surprising. In the absence of fire, L. tulipifera germination is generally inhibited by leaf litter (Lei et al., 2002; the present study). It is possible that fire promoted recruitment at our study sites by mimicking forms of litter-removing disturbance found in unburned forest. Thus, the response to cool fires may be incidental rather than an evolved behavior. L. tulipifera seeds were abundant and germination was common in our plots suggesting that availability of microsites, rather than seed, limits L. tulipifera recruitment. Although fire is not essential to germination, fire apparently improved microsite suitability by reducing litter. Our findings are in agreement with a study of burned forest sites in North Carolina in which L. tulipifera dominated seedling recruitment following fire as a result of site-saturating seed fall (Vandermast et al., 2004). An annual herb, E. hieracifolia, showed a cool-fire response similar to L. tulipifera. Germination was promoted by both litter removal and cool burns, suggesting that substrate-level disturbance is the mechanism of the fire effect. Erichtites is commonly observed following fire in CHR sites (DeSelm and Clebsch, 1991; Hutchinson and Sutherland, 2000), but is also known to germinate in the absence of fire where the tree canopy is removed (Ohtsuka, 1998; Orwig and Foster, 1998). Erichtites was common in the study area despite the absence of recent fire, and Schelling (2006) reports it is abundant in the seedbank at these sites, indicating that opportunities for establishment and reproduction are plentiful in the absence of fire. The response to fire appears to reflect adaptation to
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recruitment in litter-removing non-fire disturbances. As with Liriodendron, fire evidently provides a local opportunity for Erichtites, which is abundant but microsite-limited. Carex and Panicum spp. were very abundant in experimental plots on ridges, reflecting both germination and resprouting following treatments. Strong germination and vigorous resprouting are consistent with responses to fire reported elsewhere (Elliott et al., 1999; Taft, 2003; Hutchinson et al., 2005), but graminoid frequencies in our study were not clearly separable among treatments, so we cannot generalize about this group. In contrast to the above species, recruitment of A. rubrum was suppressed at both fire intensities. Our findings support the conclusion that fire inhibits colonization by this species (Abrams, 1998; Elliott et al., 1999). Fire may suppress seedling establishment by heat-killing dormant seeds, or by providing unsuitable habitat for germination or seedling survival. We were unable to determine the mechanism of fire response, except to rule out litter removal, fire intensity, and soil pH as controlling factors. A. rubrum was the only species that showed a strong negative correlation with the fire intensity axis, and it appears to be something of an exception in this community. 4.2. Species not responding to fire The majority of species recorded in the plots showed little response to fire. The forest herbs Onoclea sensibilis, P. simplex, Uvularia perfoliata, and Dioscorea quaternata, for example, were all common in the study sites but showed only weak correlations with the NMS axis separating treatments. In contrast to the fire-responding species described above, most non-responding species were long-lived forest herbs and shrubs typical of undisturbed forest. Non-responders were characterized by short-range dispersal, little dormancy, relatively low fecundity, individual genet longevity, and considerable shade tolerance (Matlack, 1994; Cain et al., 1998; Whigham, 2004; Schelling, 2006). Lack of a germination response in these species may reflect the absence of a soil seed bank, or failure to use environmental variation as a germination cue. Many species in the study area have soilprotected buds, but did not increase sprouting in response to fire as commonly observed in pyrophyllic communities (Matlack et al., 1993a,b; Matlack, 1997; Drewa et al., 2002). If sprouting after fire reflects heat activation of buds (Flinn and Pringle, 1983), our experimental burns may not have generated enough heat to trigger the resprouting response. Alternatively, possession of soil-protected buds may not be sufficient to insure post-fire sprouting. If growth of protected buds reflects release from suppression by active meristems (Matlack, 1997), it is possible that forest species were insensitive to fire simply because few had above-ground stems on the date when treatments were applied. It is somewhat surprising that V. pallidum, a clonally propagating shrub which appeared occasionally in our plots, showed no sprouting response to fire or fire surrogate treatments. V. pallidum has been observed to resprout in a mixed-oak forest
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in of North Carolina (Elliott et al., 1999), although densities appear to have been higher in that study. 4.3. Interactions with landscape gradients Landscape position interacted with fire and fire surrogate treatments, leading to stronger treatment effects on ridges than in valleys. The contrast may be explained by the hotter fire temperatures recorded on ridges (Glasgow and Matlack, 2007) possibly caused by drier fuels in these sites. Within sites, heterogeneity in fuel loading, moisture, slope, and wind exposure typically lead to local variation in fire intensity (Gibson and Good, 1987; Franklin et al., 1997). Such variation can be expected in any large burn in the CHR. In the present study, individual fire treatments resulted in contrasting vegetational responses, suggesting that fire at the landscape scale will create a fine-grained patchwork of opportunities for post-fire regeneration. Introduction of prescribed fire to the long- unburned CHR landscape may change the spatial organization of the forest community, introducing a novel pattern of floristic heterogeneity reflecting the local pattern of fire intensity. The effects of fire diminished through the course of the first growing season and were not detected in the second season. Declining effects of fire may be due to late-season seedling mortality observed in R. glabra, L. tulipifera, E. hieracifolia, and P. americana, which experienced large flushes of germination immediately following burning. In a similar study in a sandy forest in Illinois, Nuzzo et al. (1996) found that species richness and herb abundance diminished one year following fire because many annual species which initially responded to fire failed to regenerate in its absence. In central Florida scrub, the density of obligate seeders that germinated immediately following fire decreased rapidly due to canopy closure (Weekley and Menges, 2003). Thus, a single fire may not create permanent changes in the CHR understory community. 5. Conclusion These results suggest that fire introduced to the deciduous forest of southeastern Ohio has the potential to change understory composition by increasing germination of disturbance-adapted species from the seedbank. This is in agreement with other studies of fire in the eastern deciduous forest (DeSelm and Clebsch, 1991; Nuzzo et al., 1996; Arthur et al., 1998; Hutchinson and Sutherland, 2000; Taft, 2003). The contrast with frequent-fire communities of adjacent regions is instructive. Whereas the pyrophylic pine and scrub communities of the southeastern United States show many responses easily interpreted as adaptations to frequent fire (Platt et al., 1988; Menges and Hawkes, 1998; McConnell and Menges, 2002), species in our study sites apparently respond through adaptations to non-fire canopy disturbance. It appears that our experimental burns have favored a subset of the present community which are pre-adapted to fire through seed dormancy, high fecundity, effective dispersal, and germination
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responses to warmth and litter removal. To some extent, the observed responses may be a function of the season (midspring) when treatments were applied; other effects may occur with burns at other dates or with repeated burning. Although the effects reported here seem comparatively modest and transient, these results demonstrate that fire has the capacity to alter the flora, particularly on ridges. They suggest the direction of change which would occur with repeated and widespread burning, and highlight interactions with natural gradients in the community. Acknowledgements We thank the USFS Northeast Experiment Station for permission to use the Vinton Furnace sites. Dan Yaussy and David Hosak provided logistical support at several stages of the project. We are grateful to Peter Schweizer, John Graham, Dawn McCarthy, and Lisa Schelling for assistance in setting up treatments. Matt Dickinson, Todd Hutchinson, Brian McCarthy, and two anonymous reviewers made helpful comments on the manuscript Appendix A Most-common species in experimental plots, Vinton Furnace Experimental Forest, Vinton County, Ohio. Table includes all species which were present in 10 plots on at least one sampling date and represented by 20 individuals. Columns show the maximum frequency observed at any date, and maximum mean density in occupied plots. Species
Frequency (plots)
Density (stem/m2)
Growth Form
Acer rubrum Liriodendron tulipifera Smilax rotundifolia Erechtites hieracifolia Rubus spp. Sassafras albidum Carex sp. 1 Viola sororia Quercus alba Desmodium nudiflorum Smilax tamnoides Vitis aestivalis Galium triflorum Rhus glabra Uvularia perfoliata Vaccinium pallidum Rosa carolina Parthenocissus quinquefolia Potentilla simplex Lysimachia quadrifolia Panicum commutatum Pilea pumila Panicum sp. 1 Scutellaria serrata Circaea lutetiana Quercus prinus Arisaema atrorubens Phytolacca americana
90 72 70 58 57 57 47 43 40 37 32 32 28 27 26 25 25 20 19 18 18 18 16 16 16 16 14 13
17.20 11.68 3.53 6.04 10.32 4.51 6.83 13.24 2.89 12.74 3.30 54.71 10.89 11.27 15.96 7.40 3.80 3.38 13.00 3.47 30.36 37.33 23.91 7.45 8.31 2.88 7.5 5.33
Tree Tree Shrub Herb Shrub Tree Herb Herb Tree Herb Shrub Vine Herb Shrub Herb Shrub Shrub Vine Herb Herb Herb Herb Herb Herb Herb Tree Herb Herb
Appendix A (Continued ) Species
Frequency (plots)
Density (stem/m2)
Growth Form
Geranium maculatum Toxicodendron radicans Oxalis violacea Polystichum acrostichoides Carex sp. 2 Passiflora incarnata Osmunda cinnamomea Cimicifuga racemosa Geum spp. Ulmus americana Dioscorea quaternata Deparia acrostichoides Brachyelytrum erectrum Quercus coccinea
13 13 12 12 12 12 11 11 11 11 11 10 10 10
3.54 2.50 11.07 15 10.43 2.50 11.20 3.09 2.78 6.27 2.38 40.90 8.11 3.78
Herb Vine Herb Herb Herb Vine Herb Herb Herb Tree Herb Herb Herb Tree
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Prescribed burning and understory composition in a temperate deciduous forest, Ohio, USA Lance S. Glasgow, Glenn R. Matlack * Environmental and Plant Biology, Porter Hall, Ohio University, Athens, OH 45701, USA Received 24 June 2006; received in revised form 30 August 2006; accepted 30 August 2006
Abstract Since the advent of widespread suppression in the mid-20th century, fire has been relatively rare in deciduous forests of the eastern United States. However, widespread prescribed burning has recently been proposed as a management tool to favor oak (Quercus spp.) regeneration. To examine the potential effects of fire introduction on the understory community, we experimentally burned small plots and simulated aspects of fire at a forested site in southeastern Ohio. Treatments included two burn intensities, litter removal, increased soil pH, and a control. Treatments were arranged in a randomized block design in two landscape positions (dry upland and moist lowland) and two canopy conditions (gap, no gap). Postfire vegetation was identified to species, and stems were counted 1, 3, and 14 months after burning. Community composition was more strongly affected by fire in upland plots than in lowlands, but was not affected by canopy openness. Both cool and hot burns reduced post-fire seedling emergence of Acer rubrum, a common overstory tree. Hot burns facilitated germination of Vitis spp., Rhus glabra, and Phytolacca americana, species common in disturbed habitats, and increased graminoid abundance. Cool burns and litter removal facilitated germination of Erechtites hieracifolia and Liriodendron tulipifera suggesting that litter removal is the mechanism by which fire favors colonization. These results suggest that fire applied frequently in the Central Hardwoods Region would cause compositional shifts to graminoids and disturbance-adapted forbs by increasing germination from the seed bank. Fire did not favor species with dormant underground buds, as studies in other ecosystems would suggest. Vegetational responses were noticeably weaker in the second year after burning, indicating that a single fire has only a short-term effect. # 2006 Elsevier B.V. All rights reserved. Keywords: Forest herbs; Prescribed fire; Central Hardwoods Region
1. Introduction If fire is introduced to a long-unburned Central Hardwoods forest for management purposes, what will the consequences be for the native flora? If fire has been historically common in the region, as some studies suggest, we can expect the present flora to consist of species which tolerate regular burning. In fact, many Central Hardwoods species have growth forms and life histories which appear to pre-adapt them to tolerate fire. The history of fire in the region is not clear, however, and it is difficult to predict the fire responses of herb and shrub species based on life history, alone. If fire management is based on a misunderstanding of plant life history, or on an incorrect reading of the historical record, burning could potentially have large effects on forest community diversity. Thus, there is a need to assess the community-level implications of prescribed
* Corresponding author. Tel.: +1 740 593 1131; fax: +1 740 593 1130. E-mail address: [email protected] (G.R. Matlack). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2006.08.344
burning in Central Hardwoods forests. The question has some urgency because widespread prescribed burning has been proposed as a management tool to encourage oak regeneration (Abrams, 1992; Sutherland et al., 2003a). The fire history of the Central Hardwoods Region (CHR) is poorly understood. Today, fire rarely occurs in deciduous forests of the CHR (Yaussy and Sutherland, 1994; Lafon et al., 2005), but fire scar records show that some oak-dominated stands burned regularly in the late 19th and early 20th centuries (Sutherland, 1997; Shumway et al., 2001; Guyette and Spetich, 2003; Soucy et al., 2005; McEwan, 2006). Mean return times were as little as 5.4 years in some sites. Clearly fire has been a frequent event in some parts of the landscape, but it is difficult to generalize to the region as a whole or to a broader time scale. It is possible that natural ignition only occurs on a scale of centuries in some areas, and that much of today’s forest flora has not evolved to tolerate fire. Consistent with a low fire frequency, the modern flora does not show adaptations commonly associated with fire such as serotiny, epicormic sprouting, or a germination requirement for bare mineral soil. It
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is unclear how a flora lacking such adaptations would respond to the introduction of fire. 1.1. Fire in today’s forest Fires in the modern CHR forest tend to be of low intensity with flame lengths rarely greater than 1 m in height, and are usually confined to surface fuels (Elliott et al., 1999; Iverson and Hutchinson, 2002). Such fires typically remove a portion of the leaf litter and increase calcium available in the soil (Boerner et al., 2003; Hutchinson et al., 2005). Herb species richness, diversity, and cover have been shown to increase following fire in the region (Nuzzo et al., 1996; Arthur et al., 1998; Hutchinson and Sutherland, 2000; Kuddes-Fischer and Arthur, 2002). In Appalachian mixed-oak forests, increases in herbaceous richness and cover have been correlated with a decrease in woody plant cover, suggesting a response to light (Elliott et al., 1999; Kuddes-Fischer and Arthur, 2002; Vandermast et al., 2004). Post-fire increases in species diversity have usually been small, however, and compositional changes typically last no more than 1–2 years (Nuzzo et al., 1996). Although little is known about the fire responses of individual herb and shrub species in the region, it is possible to predict responses based on growth form and life history. The CHR herb layer is dominated by perennial species sprouting annually from buried tubers or rhizomes (Bierzychudek, 1982; Whigham, 2004). Many shrubs have the capacity to regrow from rhizomes or root crowns. In fire-prone ecosystems, shrub and perennial herb species often rely on soil-protected buds to resprout quickly following fire (Platt et al., 1988; Matlack et al., 1993a,b). Buds have been observed to initiate growth in response to a fire’s heat (Flinn and Pringle, 1983), mortality of apical meristems (Matlack, 1997), or exposure of bare soil (Platt et al., 1988). Although the dormant below-ground buds of many CHR species have not necessarily evolved in response to fire, possession of protected buds may allow them to reestablish quickly after fire. Sprouting capacity may pre-adapt many herb and shrub species to survive prescribed fires with little negative effect. 1.2. Seed germination In fire-prone ecosystems, fire is often followed by a flush of germination from the seed bank (Lemon, 1949; Keeley et al., 2003; Milberg and Lamont, 1995; Morgan, 2001). Seed banks in deciduous forest sites are generally small relative to those of other North American ecosystems (Harper, 1977), and typically include disturbance-oriented annual and perennial herb species (Matlack and Good, 1990; Hyatt and Casper, 2000; Schelling, 2006). Fire appears to have the potential to cue germination in some of these species. In mixed hardwood forest of southeast Ohio, several species have been observed to colonize burned sites by germination from seed, including Rubus spp., Rhus glabra, Vitis spp., Phytolacca americana, Erechtites hieracifolia, Carex spp., Panicum spp., and Eupatorium rugosum (Hutchinson and Sutherland, 2000; Vandermast et al., 2004; Hutchinson et al., 2005). These species are normally found in
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forest edges, treefall gaps, and other non-fire disturbances, suggesting that fire may encourage them through its impact on canopy openness and soil disturbance. We predict that prescribed burning would cause a compositional shift to such species by promoting seedling recruitment. Removal of live and dead vegetation often triggers germination in fire-prone communities. In Florida oak scrub, for example, the colonization dynamics of understory species are largely controlled by fire-formed gaps in the dominant shrub layer; several endemic species are only found in these gaps (Menges and Hawkes, 1998). Mechanical removal of vegetation or litter has been shown to produce vegetational effects similar to fire in such communities (Greenberg et al., 1995; McConnell and Menges, 2002). In the absence of fire, vegetation and litter often inhibit germination by preventing seed contact with soil and blocking light necessary for germination (Klinkhammer and Jong, 1988; Fowler, 1988; Xiong and Nilsson, 1999; McConnell and Menges, 2002; Vickery, 2002). Presumably, fire would act on vegetation in the CHR by removing litter and vegetational inhibition, thereby promoting recruitment. Seedling germination and survival might be further enhanced by release of nutrients following fire (Romanya et al., 1994). We report a small-plot experiment designed to test the fire effects postulated above. Natural vegetation in a CHR forest site was subjected to fire and two fire surrogate treatments. The small size of individual plots allowed a high degree of control over the intensity and uniformity of treatments, and allowed a precise spatial linkage of treatments and vegetation response. Interactions were examined between treatments and landscape position and canopy openness, two important non-fire factors shaping vegetation in this community. Because understory species may vary widely in their responses to fire, we considered species responses individually. Based on observations in other plant communities (above), we hypothesized that fire in a CHR site would favor seedbank species and species able to propagate from protected meristems. We expected fire to control germination through litter removal, reasoning that litter accumulation would impede seedling establishment (Xiong and Nilsson, 1999; McConnell and Menges, 2002; Vickery, 2002). Germination is also known to respond to heat and smoke in some cases (Brown and van Staden, 1997; Bellairs et al., 2006). Because all of these effects are dependent on fire exposure, the effects of fire were expected be greater in more intense burns, and to vary with landscape position and canopy openness to the extent that these factors influence local fire intensity. 2. Methods 2.1. Study area Experimental plots were established in the Vinton Furnace Experimental Forest (VFEF) (398110 N, 828220 W) on the unglaciated Alleghany Plateau of southeastern Ohio, USA. The study area is adjacent to the Ohio Hills site of the US Forest Service’s Fire and Fire Surrogate experiment (Iverson et al., 2004), and our treatments were designed to mimic treatments in
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that study. The area is dissected by narrow ridges and small valleys with elevations ranging from 200 to 300 m a.s.l (Brockman, 1998). Soils are moderately to well-drained sandy and silt loams derived from sandstone, siltstone, and shale (Lemaster, 2004). Southeastern Ohio has a humid-continental climate, with an average annual temperature of 11.3 8C and annual precipitation of 1024 mm (NOAA, 2004). Natural vegetation is a mixed deciduous forest characteristic of the Low Hills section of the Allegheny Plateau (Braun, 1950). Valley sites are relatively moist with canopies dominated by Acer saccharum, Nyssa sylvatica and Liriodendron tulipifera. Ridges and south-facing slopes are drier and dominated by Quercus spp., Carya spp., and A. rubrum. Understory community composition is largely determined by topographic position (Small and McCarthy, 2002) and canopy openness (Hughes and Fahey, 1991; Reader and Bricker, 1992). All sites used in this study were cleared for fuelwood in the 19th century, but were not cultivated. Sites are now covered with long-established second growth forest. The ground flora is generally species-rich with a well-developed herbaceous community. Surveys of fire scars show that two nearby stands burned often between ca. 1870 and 1930, but that fire was usually limited to dry ridges and upper slope positions (Sutherland, 1997; Hutchinson and Sutherland, unpublished). Those fires were probably anthropogenic in origin (Yaussy and Sutherland, 1994). There is no record of fire at the sites used in the present study, and the study area has been fire-free for several decades at least. Experimental plots were established in apparently homogeneous, level microsites which included no plant stems >1 cm diameter. A comparison with randomly chosen microsites in adjacent forest (Glasgow and Matlack, 2007) found no significant difference in any of fifteen edaphic and vegetational variables, suggesting that the experimental sites were typical of forest in their respective landscape positions. Herbaceous species were dormant when plots were established in December 2003, so the richness and stem density of individual plots was not known beforehand. Occasional woody stems were clipped at ground level. 2.2. Treatments Treatments were applied in five 2 m 2 m permanent plots at each site. To asses the effects of prescribed fires on establishment of understory vegetation, plots in the cool burn treatment were burned using only the pre-existing leaf litter as fuel. A fine mist of kerosene was sprayed on the fuel beforehand to ensure uniform ignition. Temperatures in burn treatments were monitored with pyrometer tags marked with temperaturesensitive paint (Glasgow and Matlack, 2007). Temperatures at the soil surface ranged from 84 to 195 8C, with flame lengths of 5–15 cm. Prescribed burns in deciduous forest tend to be patchy, varying in intensity according to local fuel loading, moisture, and slope (Gibson and Good, 1987; Franklin et al., 1997), and some microsites within the fire perimeter experience temperatures much higher than the average value. To simulate the effects of hotter burns on the understory flora, we increased
fuel loading by adding twenty air-dry pine furring strips (3 cm 3 cm 200 cm) in the hot burn treatment. Pine strips were evenly spaced on top of the existing leaf litter. Paint tags in the hot burns consistently reached 150–230 8C hotter than those in cool burns. These temperatures are comparable to average and extreme values recorded in prescribed burns in the study area (Iverson and Hutchinson, 2002). Flame lengths varied from 10 to 30 cm. To test litter removal as a mechanism by which fire effects understory plant recruitment, leaf litter was removed by hand down to the humic layer simulating the effect of a ground-level fire (litter removal treatment). Caution was used not to disturb the humic soil surface. In the fourth treatment, agricultural lime was added to simulate nutrient addition from ash (lime addition). In deciduous forests of southeastern Ohio, the most significant change in soil chemistry following fire is an increase in calcium and elevation in soil pH (increasing from ca. 3.8 to 4.2 units; Boerner et al., 2003, Boerner, personal communication). Lime was added as needed to contribute Ca and to raise the pH in each plot 0.4 units (Glasgow and Matlack, 2007). Finally, a control treatment with no manipulation was also established. Treatments were applied between April 5th and April 9th, 2004, to coincide with burn treatments in the nearby Fire and Fire Surrogate study (Iverson et al., 2004). 2.3. Experimental design A factorial design was used to test the effects of fire, canopy openness, and landscape position on understory vegetation. The five experimental treatments were applied in each of 20 sites in a forested area of ca. 2000 ha. All sites were situated at least 50 m from roads and other large openings to avoid edge effects (Matlack, 1993, 1994), and at least 250 m from other sites to ensure statistical independence. To test how canopy openness and landscape position interact with fire, sites were established in two landscape positions (ridge tops and valleys) and in two canopy conditions (open and closed). Valley plots were located on terraces beside small streams. Open-canopy sites were selected in natural canopy openings. Small trees and saplings were felled as needed to ensure a minimum canopy openness of 40% measured at a central point. Each landscape position canopy-openness combination was replicated five times, giving a total of 100 plots in twenty sites. Landscape canopy combinations were evenly distributed across the study area. All vascular plants emerging after treatment were identified to species following Gleason and Cronquist (1991). Stem number was recorded by species in July and September 2004 to quantify mid- and late-summer response, respectively, and in June 2005 to test vegetation response one year following fire. In each plot, all data were collected in a centered 1 m2 sub-plot to avoid variation at plot edges. 2.4. Analysis Nonmetric multidimensional scaling (NMS) was used to assess trends in species composition at all sample dates (PCORD, MJM Software, Gleneden Beach, Oregon). NMS is a
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non-parametric iterative ordination technique well suited for non-normal data sets typical of ecological studies (McCune and Grace, 2002). NMS uses ranked distances to ordinate experimental plots in species space along a series of axes determined by a minimum stress configuration (a measure of departure from monotonicity). NMS was run on data from each sample date using Bray–Curtis distance measures, four axes, 200 iterations, and an instability criterion of 0.0001. A Monte Carlo test was used to determine the minimum number of dimensions required to yield the lowest stress. A threedimensional solution was deemed appropriate for all data sets. A randomized complete block ANOVA was performed on species richness, Shannon–Weiner diversity (H0 ), and total stem number in each plot. Canopy openness, landscape position, and treatment were included as main effects. Species correlated with NMS axis scores (r > 0.45) were reanalyzed individually within the respective landscape positions to detect individual responses to treatments and canopy openness. ANOVA of stem number was followed by a Tukey–Kramer multiple comparison test to determine significant differences among treatments. 3. Results A total of 72 forbs, 6 ferns, 35 woody species, and 7 graminoids were identified in experimental plots between July 2004 and June 2005 (Appendix A). Stem density and species frequency across all plots were dominated by three taxa: A. rubrum, L. tulipifera, and Rubus spp. Smilax rotundifolia, Carex sp. 1, and Desmodium nudiflorum were widely present at low levels, but showed high densities in individual ridge plots. Likewise, high densities of Pilea pumila, Deparia acrostichoides, and Panicum commutatum were recorded in several
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valley plots. Species richness and total stem density were significantly greater in valleys than on ridges for all sample dates (Fig. 1). Species diversity (H0 ; not shown) showed the same pattern of significance as richness ( p < 0.05). Stem density was significantly greater in canopy openings than under closed canopies in September 2004 and June 2005. Richness was significantly greater under closed canopies than in gaps in July 2004 but the difference decreased at later dates and was not statistically significant (Fig. 1). Diversity was not significantly affected by canopy openness. Fire and fire surrogate treatments had little effect on total stem density, species richness, or diversity (ANOVA, P > 0.05). 3.1. Species composition Landscape position separated plots along the first NMS axis in July 2004 (33.2% of variation) and September 2004 (Fig. 2; 30.8% of variation) and along axis 2 in June 2005 (31.4% of variation). In each case, the axis most clearly separating landscape positions explained the greatest variation in the analysis. Most of the species which correlated strongly with axis 1 in July 2004 and axis 2 in June 2005 were understory herbs typical of valleys (Table 1). In September 2004, woody species were also strongly correlated with the ridge-valley axis: R. glabra was primarily found in valleys, while A. rubrum and Sassafras albidum were associated with ridges. Because ridge and valley communities differed markedly in composition, plots in the two communities were re-analyzed separately to test for compositional effects of canopy openness. NMS showed separation between open and closed canopies within both ridge and valley sites in September 2004 (Fig. 3), but canopy types were more clearly separated on ridges. In
Fig. 1. Comparisons of stem density and species richness between landscape positions and canopy openness. Error bars represent the standard error. An asterisk (*) indicates a significant difference in overall ANOVA between valleys and ridges or open and closed canopies. Significance: *P < 0.05; **P < 0.01; ***P < 0.001.
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(r = 0.49) was predominantly found in gaps. Canopy openness effects were less apparent in July 2004 and June 2005. 3.2. Fire and fire surrogate treatments
Fig. 2. Ordination of plots by species in nonmetric multidimensional scaling (NMS), September 2004. Axis 1 accounts for 30.8% of the of the total variation explained by the analysis. The convex polygons encompass all Ridge and Valley sites, respectively. The ellipse indicates an outlying Ridge site. Ordinations from all other sample dates show similar degrees of clustering. Codes: ‘‘c’’ as a first letter, closed canopy; ‘‘o’’, open canopy; ‘‘c’’ as a second letter, control; ‘‘cb’’ as second and third letters, cool burn; ‘‘hb’’, hot burn; ‘‘l’’, litter removal; ‘‘f’’, lime addition.
valley communities in September 2004, plots were separated by canopy openness along axis 1 (20.6% of variation; Fig. 3a). The understory herbs Asarum canadense (r = 0.52), Galium triflorum (r = 0.62), Potentilla sp. 1 (r = 0.501), and Potentilla simplex (r = 0.51) were negatively correlated with scores on the first axis indicating abundance under closed canopies, while the woody species A. rubrum (r = 0.51), and L. tulipifera (r = 0.55) were positively correlated, indicating presence in canopy gaps. In ridge communities plots were separated by canopy openness on axis 3 (33.0% of variation) (Fig. 3b). D. nudiflorum (r = 0.59) and R. glabra (r = 0.48) were strongly associated with low values on the third axis indicating preference for a closed canopy, while Pinus sp. Table 1 Pearson product-moment correlations (r > 0.45) of species abundance with scores on NMS axes which most strongly separated plots by landscape position Taxa Acer rubrum Cimicifuga racemosa Circaea lutetiana Cardamine concatenata Galium triflorum Pilea pumila Potentilla sp. 1 Rhus glabra Sassafras albidum Viola sororia
July 2004, axis 1
September 2004, axis 1
June 2005, axis 2
0.497 0.508 0.523 0.513 0.617 0.518
0.649
0.754 0.490 0.530 0.465 0.688
Positive correlation coefficients indicate higher densities in valleys.
Because there is a strong a priori reason to expect a separation of species composition by landscape position, and such an effect is demonstrated above, compositional effects of fire and fire surrogate treatments were examined separately for ridge and valley sites. In ridge communities, plots were clearly separated by treatments along axis 2 in July 2004 (40.2% of variation) and axis 1 in September 2004 (21.1% of variation) (Fig. 4). Hot burn plots on ridges tended to be dominated by graminoids in both density and frequency, including Carex sp. 1 (likely C. wildenovii), P. commutatum and Panicum sp. 1 (likely P. dichotomum), arising as both seedlings and vegetative shoots. Woody species were also frequently observed in hot burns, including L. tulipifera, Rubus spp., R. glabra and Vitis spp.. Abundance of R. glabra, Carex sp. 1, P. americana, L. tulipifera, and Rubus spp. on ridges showed positive correlations with scores on axes separating treatments (Table 2), suggesting these species were favored by fire. A. rubrum showed a negative correlation with axes in July and September, respectively, suggesting that abundance of this species declines with fire. Separation between treatments was less distinct in September 2004 than in July, and was no longer apparent in 2005, indicating that the effects of fire on ridge community composition persisted less than a year. Species that showed moderate to strong correlations (r > 0.45) with NMS axes were analyzed by ANOVA within landscape positions, with canopy openness and treatment as main effects. Canopy openness was not significantly related to frequency in any of the species date landscape position combinations examined, thus, only F-values for the treatment term are reported. In ridge communities in July, stem number of A. rubrum was significantly greater in non-burn treatments than in burn treatments (F = 4.80, d.f. = 4, P < 0.01; Tukey–Kramer multiple comparison test P < 0.05). Stem number of R. glabra was significantly greater in the hot-burn treatment than in all other treatments (F = 7.93, d.f. = 4, P < 0.001; Tukey–Kramer P < 0.05), suggesting that fire intensity is critical to recruitment in this species. L. tulipifera seedlings were significantly more abundant in cool burn treatments than in the control, lime addition, or hot burn treatments (F = 10.43, d.f. = 4, P < 0.0001; Tukey–Kramer P < 0.05), but cool burns were not distinguishable from the leaf litter treatment, implying that fire acts on Liriodendron recruitment by removal of leaf litter. Presence of cotyledons on most individuals of these species indicates that regeneration was primarily caused by germination. In September 2004 no taxa were significantly affected by treatments or canopy openness on ridges (ANOVA, P 0.05). In valley communities separation among treatments was not as distinct as on ridges, only appearing in July 2004 (24.5% of variation, axis 3, not shown). In the ordination, hot burns were distinct from non-burn treatments, and cool burns were transitional between hot burns and all other treatments. P. americana showed a strong positive correlation with axis 3 in
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Fig. 3. Ordination of plots in (a) valleys and (b) ridge-top sites according to total species composition in September 2004 by nonmetric multidimensional scaling (NMS). Convex polygons include all gap and no gap sites, respectively. Circles represent outliers in the open and closed canopy data in the valley community. Codes: ‘‘c’’, control; ‘‘cb’’, cool burn; ‘‘hb’’, hot burn; ‘‘l’’, litter removal; ‘‘f’’, lime addition.
valley communities (Table 2), indicating that this species increased following fire. As in ridge communities, A. rubrum showed strong negative correlation with axis 3, again suggesting that fire inhibits germination or seedling survival. When analyzed individually, stem number of A. rubrum in valleys was found to be significantly greater in control plots than in lime addition, cool burn or hot burn treatments (F = 7.17, d.f. = 4, P < 0.001; Tukey–Kramer P < 0.05). A significantly greater number of P. americana seedlings were observed in hot burns than in other treatments, suggesting that germination of P. americana in valleys is controlled by fire intensity (F = 5.38, d.f. = 4, P < 0.01; Tukey–Kramer P < 0.05). Neither A. rubrum nor P. americana responded to canopy openness in valleys (ANOVA, P > 0.05). The responses of Vaccinium pallidum, E. hieracifolia, and Vitis spp. to fire were examined individually because these species have been shown to respond positively in other studies in the region (Elliott et al., 1999; Hutchinson and Sutherland, 2000). Landscape position, canopy openness, and treatment were included as main effects. E. hieracifolia was significantly influenced by treatments in July 2004 (ANOVA, Table 2 Correlations of species abundance with scores on NMS axes which most strongly (r > 0.45) separated plots by experimental treatment Taxa Rhus glabra Carex sp. 1 Phytolacca americanaa Liriodendron tulipifera b Rubus spp. Acer rubrum Acer rubruma
July 2004, axis 2
September 2004, axis 1
0.722 0.621 0.483 0.563 0.533 0.721 0.772
0.722
Positive correlations indicate higher densities in burned plots. Ridge and valley data are considered separately. a Distributions in valley sites; the remainder describe ridge communities. No correlations of r > 0.45 were recorded in June 2005. b Measured in August 2004.
F treatment = 15.05, d.f. = 4, P < 0.0001). Stem number was significantly higher in cool burn treatments than in hot burns, lime addition, or control treatments; and significantly greater in litter removal treatments than in control and lime addition treatments (Tukey–Kramer P < 0.05). Stem number of Vitis spp. was significantly higher in hot burns than in control, lime addition and leaf litter removal treatments (F treatment = 3.55, d.f. = 4, P < 0.05; Tukey–Kramer P < 0.05) and greater in uplands than valleys (F landscape = 7.09, d.f. = 1, P < 0.01). Almost all Vitis individuals were seedlings, as indicated by presence of cotyledons, implying that hot burns facilitate germination of this species. ANOVA detected no significant differences in stem density for V. pallidum. Neither Vitis spp., E. hieracifolia, nor V. pallidum responded to canopy openness (ANOVA, P > 0.05). Data recorded in the June 2005 were not analyzed because NMS failed to show separation among treatments. 4. Discussion Landscape position and canopy gaps are major factors structuring vegetation in deciduous forests of the eastern United States (Hughes and Fahey, 1991; Reader and Bricker, 1992; Olivero and Hix, 1998; Small and McCarthy, 2002) and they were important in our sites. Valley plots contained more stems and more species than ridge plots and were largely distinct in understory composition, a contrast which created a twocommunity background for the fire treatments. Canopy openness led to greater collective stem density, lower richness at some dates, and abundance of some individual species, although many widely recognized gap-occupying species showed no response. Failure to respond suggests that the openings used here were too small to substantially change the forest microclimate. Experimental burning caused changes in understory composition, effects most clearly evident in the ridge sites. Fire effects were evident despite considerable patchiness in the herb flora and the potential interaction of patchiness with small plot size. Many stems were observed in
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Fig. 4. Ordinations of ridge-top sites showing separation among treatments. Convex polygons each enclose all sites in a particular treatment. Circles indicate outliers in the hot and cool burn clusters. Ordinations are not shown for the 2005 data sets because NMS did not distinguish compositional differences between treatments. Codes: ‘‘o’’, open canopy; ‘‘c’’, closed canopy.
most experimental plots. Species recorded in plots included most of those growing in the immediate area, and many of the most common forest herb and shrub species in the region. Thus, we assume these results offer a fair description of the potential impact of fire in this forest community. 4.1. Life histories of fire responders Four types of fire response can be recognized among the species examined here. Emergence of shoots was either inhibited by fire, facilitated by hot fires, facilitated by cool fires and removal of leaf litter, or apparently unaffected. Addition of lime did not appear to influence emergence of forest species. We conclude that fire-caused changes in pH and Ca are not related to the vegetational effects reported here. Three taxa, R. glabra, Vitis spp., and P. americana, illustrate the response to fire intensity, with germination facilitated by hot burns but showing little response to cool burns or litter removal. Germination of each species was consistent with post-fire performance in other studies in CHR forests (DeSelm and Clebsch, 1991; Hutchinson and Sutherland, 2000; Vandermast et al., 2004). More commonly, all three taxa regularly establish in open sites in the absence of fire (Luken et al., 1997; Hyatt and Casper, 2000), demonstrating that germination can also be caused by non-fire disturbance. Germination of R. glabra has been shown to increase when seeds are warmed (Shelton and Cain, 2003) possibly reflecting adaptation to solar warming as a germination cue. Vitis spp. can germinate in canopy openings in which litter and soil are not disturbed (Haywood, 1994; Luken et al., 1997), again consistent with solar warming. Thus, the response to high-intensity fire appears to parallel a non-fire response to canopy disturbance. Sensitivity to soil warmth, a useful gauge of canopy openness in non-fire disturbances, may function as a pre-adaptation to fire intensity in burned sites. Other species responded primarily to cool fires. L. tulipifera, a common gap-occupying canopy tree (Clinton et al., 1994), showed high germination rates in both cool burn and litter-
removal treatments, suggesting that the two treatments are equivalent for the establishment of this species. Removal of leaf litter is known to be a mechanism by which fire alters community composition in other ecosystems, presumably by providing favorable microsites for seed germination (Greenberg et al., 1995; McConnell and Menges, 2002). L. tulipifera does not have any obvious adaptations to fire, however, and is largely absent from fire-shaped ecosystems of North America (Prasad and Iverson, 2006), implying a lack of evolutionary experience with fire. In this study hot burns led to decreased germination, again consistent with non-adaptation to fire, so the cool fire response observed here is surprising. In the absence of fire, L. tulipifera germination is generally inhibited by leaf litter (Lei et al., 2002; the present study). It is possible that fire promoted recruitment at our study sites by mimicking forms of litter-removing disturbance found in unburned forest. Thus, the response to cool fires may be incidental rather than an evolved behavior. L. tulipifera seeds were abundant and germination was common in our plots suggesting that availability of microsites, rather than seed, limits L. tulipifera recruitment. Although fire is not essential to germination, fire apparently improved microsite suitability by reducing litter. Our findings are in agreement with a study of burned forest sites in North Carolina in which L. tulipifera dominated seedling recruitment following fire as a result of site-saturating seed fall (Vandermast et al., 2004). An annual herb, E. hieracifolia, showed a cool-fire response similar to L. tulipifera. Germination was promoted by both litter removal and cool burns, suggesting that substrate-level disturbance is the mechanism of the fire effect. Erichtites is commonly observed following fire in CHR sites (DeSelm and Clebsch, 1991; Hutchinson and Sutherland, 2000), but is also known to germinate in the absence of fire where the tree canopy is removed (Ohtsuka, 1998; Orwig and Foster, 1998). Erichtites was common in the study area despite the absence of recent fire, and Schelling (2006) reports it is abundant in the seedbank at these sites, indicating that opportunities for establishment and reproduction are plentiful in the absence of fire. The response to fire appears to reflect adaptation to
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recruitment in litter-removing non-fire disturbances. As with Liriodendron, fire evidently provides a local opportunity for Erichtites, which is abundant but microsite-limited. Carex and Panicum spp. were very abundant in experimental plots on ridges, reflecting both germination and resprouting following treatments. Strong germination and vigorous resprouting are consistent with responses to fire reported elsewhere (Elliott et al., 1999; Taft, 2003; Hutchinson et al., 2005), but graminoid frequencies in our study were not clearly separable among treatments, so we cannot generalize about this group. In contrast to the above species, recruitment of A. rubrum was suppressed at both fire intensities. Our findings support the conclusion that fire inhibits colonization by this species (Abrams, 1998; Elliott et al., 1999). Fire may suppress seedling establishment by heat-killing dormant seeds, or by providing unsuitable habitat for germination or seedling survival. We were unable to determine the mechanism of fire response, except to rule out litter removal, fire intensity, and soil pH as controlling factors. A. rubrum was the only species that showed a strong negative correlation with the fire intensity axis, and it appears to be something of an exception in this community. 4.2. Species not responding to fire The majority of species recorded in the plots showed little response to fire. The forest herbs Onoclea sensibilis, P. simplex, Uvularia perfoliata, and Dioscorea quaternata, for example, were all common in the study sites but showed only weak correlations with the NMS axis separating treatments. In contrast to the fire-responding species described above, most non-responding species were long-lived forest herbs and shrubs typical of undisturbed forest. Non-responders were characterized by short-range dispersal, little dormancy, relatively low fecundity, individual genet longevity, and considerable shade tolerance (Matlack, 1994; Cain et al., 1998; Whigham, 2004; Schelling, 2006). Lack of a germination response in these species may reflect the absence of a soil seed bank, or failure to use environmental variation as a germination cue. Many species in the study area have soilprotected buds, but did not increase sprouting in response to fire as commonly observed in pyrophyllic communities (Matlack et al., 1993a,b; Matlack, 1997; Drewa et al., 2002). If sprouting after fire reflects heat activation of buds (Flinn and Pringle, 1983), our experimental burns may not have generated enough heat to trigger the resprouting response. Alternatively, possession of soil-protected buds may not be sufficient to insure post-fire sprouting. If growth of protected buds reflects release from suppression by active meristems (Matlack, 1997), it is possible that forest species were insensitive to fire simply because few had above-ground stems on the date when treatments were applied. It is somewhat surprising that V. pallidum, a clonally propagating shrub which appeared occasionally in our plots, showed no sprouting response to fire or fire surrogate treatments. V. pallidum has been observed to resprout in a mixed-oak forest
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in of North Carolina (Elliott et al., 1999), although densities appear to have been higher in that study. 4.3. Interactions with landscape gradients Landscape position interacted with fire and fire surrogate treatments, leading to stronger treatment effects on ridges than in valleys. The contrast may be explained by the hotter fire temperatures recorded on ridges (Glasgow and Matlack, 2007) possibly caused by drier fuels in these sites. Within sites, heterogeneity in fuel loading, moisture, slope, and wind exposure typically lead to local variation in fire intensity (Gibson and Good, 1987; Franklin et al., 1997). Such variation can be expected in any large burn in the CHR. In the present study, individual fire treatments resulted in contrasting vegetational responses, suggesting that fire at the landscape scale will create a fine-grained patchwork of opportunities for post-fire regeneration. Introduction of prescribed fire to the long- unburned CHR landscape may change the spatial organization of the forest community, introducing a novel pattern of floristic heterogeneity reflecting the local pattern of fire intensity. The effects of fire diminished through the course of the first growing season and were not detected in the second season. Declining effects of fire may be due to late-season seedling mortality observed in R. glabra, L. tulipifera, E. hieracifolia, and P. americana, which experienced large flushes of germination immediately following burning. In a similar study in a sandy forest in Illinois, Nuzzo et al. (1996) found that species richness and herb abundance diminished one year following fire because many annual species which initially responded to fire failed to regenerate in its absence. In central Florida scrub, the density of obligate seeders that germinated immediately following fire decreased rapidly due to canopy closure (Weekley and Menges, 2003). Thus, a single fire may not create permanent changes in the CHR understory community. 5. Conclusion These results suggest that fire introduced to the deciduous forest of southeastern Ohio has the potential to change understory composition by increasing germination of disturbance-adapted species from the seedbank. This is in agreement with other studies of fire in the eastern deciduous forest (DeSelm and Clebsch, 1991; Nuzzo et al., 1996; Arthur et al., 1998; Hutchinson and Sutherland, 2000; Taft, 2003). The contrast with frequent-fire communities of adjacent regions is instructive. Whereas the pyrophylic pine and scrub communities of the southeastern United States show many responses easily interpreted as adaptations to frequent fire (Platt et al., 1988; Menges and Hawkes, 1998; McConnell and Menges, 2002), species in our study sites apparently respond through adaptations to non-fire canopy disturbance. It appears that our experimental burns have favored a subset of the present community which are pre-adapted to fire through seed dormancy, high fecundity, effective dispersal, and germination
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responses to warmth and litter removal. To some extent, the observed responses may be a function of the season (midspring) when treatments were applied; other effects may occur with burns at other dates or with repeated burning. Although the effects reported here seem comparatively modest and transient, these results demonstrate that fire has the capacity to alter the flora, particularly on ridges. They suggest the direction of change which would occur with repeated and widespread burning, and highlight interactions with natural gradients in the community. Acknowledgements We thank the USFS Northeast Experiment Station for permission to use the Vinton Furnace sites. Dan Yaussy and David Hosak provided logistical support at several stages of the project. We are grateful to Peter Schweizer, John Graham, Dawn McCarthy, and Lisa Schelling for assistance in setting up treatments. Matt Dickinson, Todd Hutchinson, Brian McCarthy, and two anonymous reviewers made helpful comments on the manuscript Appendix A Most-common species in experimental plots, Vinton Furnace Experimental Forest, Vinton County, Ohio. Table includes all species which were present in 10 plots on at least one sampling date and represented by 20 individuals. Columns show the maximum frequency observed at any date, and maximum mean density in occupied plots. Species
Frequency (plots)
Density (stem/m2)
Growth Form
Acer rubrum Liriodendron tulipifera Smilax rotundifolia Erechtites hieracifolia Rubus spp. Sassafras albidum Carex sp. 1 Viola sororia Quercus alba Desmodium nudiflorum Smilax tamnoides Vitis aestivalis Galium triflorum Rhus glabra Uvularia perfoliata Vaccinium pallidum Rosa carolina Parthenocissus quinquefolia Potentilla simplex Lysimachia quadrifolia Panicum commutatum Pilea pumila Panicum sp. 1 Scutellaria serrata Circaea lutetiana Quercus prinus Arisaema atrorubens Phytolacca americana
90 72 70 58 57 57 47 43 40 37 32 32 28 27 26 25 25 20 19 18 18 18 16 16 16 16 14 13
17.20 11.68 3.53 6.04 10.32 4.51 6.83 13.24 2.89 12.74 3.30 54.71 10.89 11.27 15.96 7.40 3.80 3.38 13.00 3.47 30.36 37.33 23.91 7.45 8.31 2.88 7.5 5.33
Tree Tree Shrub Herb Shrub Tree Herb Herb Tree Herb Shrub Vine Herb Shrub Herb Shrub Shrub Vine Herb Herb Herb Herb Herb Herb Herb Tree Herb Herb
Appendix A (Continued ) Species
Frequency (plots)
Density (stem/m2)
Growth Form
Geranium maculatum Toxicodendron radicans Oxalis violacea Polystichum acrostichoides Carex sp. 2 Passiflora incarnata Osmunda cinnamomea Cimicifuga racemosa Geum spp. Ulmus americana Dioscorea quaternata Deparia acrostichoides Brachyelytrum erectrum Quercus coccinea
13 13 12 12 12 12 11 11 11 11 11 10 10 10
3.54 2.50 11.07 15 10.43 2.50 11.20 3.09 2.78 6.27 2.38 40.90 8.11 3.78
Herb Vine Herb Herb Herb Vine Herb Herb Herb Tree Herb Herb Herb Tree
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