2013 SOUTHEASTERN NATURALIST 12(1):99–120 Response of Federally Threatened Scutellaria montana (Large-flowered Skullcap) to Pre-transplantation Burning and Canopy Thinning H. Mae Kile1, Joey Shaw1, and Jennifer Nagel Boyd1,* Abstract - Federally threatened Scutellaria montana (Large-flowered Skullcap) is a perennial herbaceous species endemic to southeastern Tennessee and northwestern Georgia. A large population of S. montana is located at the 648-ha Tennessee Army National Guard Volunteer Training Site (VTS) in Catoosa County, GA. Due to necessary operational activities that include vegetation clearing along site boundaries to maintain security and prescribed burning and overstory clearing to reduce fuel loads as a wildfire-prevention measure, S. montana individuals and groups at the VTS may be disturbed unavoidably at times. Our objectives were to provide recommendations for land managers at the VTS and elsewhere regarding the response of S. montana to transplantation when plant rescue is necessary and to guide site selection for transplantation by elucidating the effects of pre-transplantation burning and canopy thinning on transplant survival and subsequent success. We relocated 100 S. montana individuals in spring 2010 from a site scheduled for clearing to plots that were burned (B), thinned (T), treated with a combination of burning and thinning (B+T), or not treated (C; control). Survival, growth, reproductive potential, development, and physiological measurements were used throughout the 2010 and 2011 growing seasons to evaluate the success of transplantation overall and in various relocation plots. At one year post-transplantation, 91% of the original transplants had survived relocation, and among all transplants, mean stem height and the numbers of stems, leaves, and flowers per individual significantly increased. Additionally, the percentage of total transplants that were juveniles was much lower one year post-transplantation than immediately following transplantation (5.7% vs. 27%), while the proportion that were reproductive adults was greater one year post-transplantation (37.5% vs. 22%). However, reduced survival was found in the canopy-thinned plots (84% in both plot T and plot B+T) compared to plot B (100%) and plot C (96%) one year post-transplantation. The main effects of both burning and thinning included significant increases in stem damage and in the proportion of transplants that were vegetative adults, with an associated decrease in the proportion of reproductive adults. Combined, these findings may have resulted from increased trampling and feeding activity of vertebrate herbivores in burned and thinned plots. Overall, we considered our transplantation efforts to be successful due to high survivability and continued growth and development of individuals one year post-transplantation. However, to maximize the success of S. montana relocation, we suggest that transplants be relocated into unburned, unthinned forests and that vertebrate herbivory be subsequently controlled though the use of exclosur es. Introduction Transplanting plants from one location to another is a process that can be used to relocate plants from areas with planned habitat modification or destruction 1The University of Tennessee at Chattanooga, Department of Biological and Environmental Sciences, Chattanooga, TN 37403. *Corresponding author - jennifer-boyd@ utc.edu. 100 Southeastern Naturalist Vol. 12, No. 1 (Fahselt 2007). However, numerous issues that could impede successful transplantation have been well documented and include proper transplantation site selection, poorly understood life histories, disturbance and stress to plants, stochastic loss of genetic diversity leading to inbreeding depression or hybridization at the transplantation site leading to outbreeding depression, high economic costs, poor survivability, and few long-term monitoring protocols (Allen 1994, Fahselt 2007, Montalvo and Ellstrand 2000, Walters et al. 1994). Some of these impacts can be minimized through methodology; however, poor conceptual planning for success goals and long-term monitoring—all identified as causes of transplantation failure—have led to some discouragement of this practice (Berg 1996). Given the potential negative outcomes of transplantation efforts, reservations concerning transplantation as a form of conservation mitigation have been voiced (Allen 1994, Fahselt 2007, Falk et al. 1996, Primack 2006, Wendelberger et al. 2008). Transplantation of plant species of special concern is especially troubling to critics, since the persistence of such species is often dependent on undisturbed, intact habitat (Fahselt 2007, Falk and Olwell 1992). In general, habitat preservation is essential to conservation efforts, because habitat destruction due to human activities is considered the primary threat to biological diversity (Primack 2006). Since habitat destruction has not yet been abated as a practice, and when the alternative is plant loss in a condemned area, transplantation is an option for the rescue of at-risk plants (Fahselt 2007, Falk and Olwell 1992, Wendelberger et al. 2008). For mitigation to be successful, projects must move beyond the traditional view of success, in which transplants are expected to survive for only a few years, into an ecological view of success where transplants become a viable, self-maintaining population reflecting natural communities (Fahselt 2007, Jusaitis 2005, Pavlik et al. 1993, Primack 1996). The latter perspective requires long-term monitoring of survival, reproduction, seedling establishment to recruitment, and population viability estimations in comparison to natural reference populations (Menges 2008, Primack 1996). Since transplantation mitigation can be costly and characterized by low success, small-scale transplantation experiments can guide the feasibility of such action and help avoid some of its common pitfalls (Jusaitis 2005). This transplantation study was prompted by unavoidable vegetation clearing at the Tennessee Army National Guard (TNARNG) Volunteer Training Site (VTS), in Catoosa County, GA, that would drastically disturb the existing habitat of Scutellaria montana Chapm. (Large-flowered Skullcap). Scutellaria montana is an herbaceous perennial species found in scattered populations in the Ridge and Valley physiographic province and the eastern escarpment of the Cumberland Plateau, including known populations in nine counties in northwestern Georgia and four in southeastern Tennessee (USFWS 2012). This rare species was listed in 1986 as federally endangered under the United States Endangered Species Act, but it was reclassified as federally threatened in 2002. Currently, S. montana also is considered endangered at the state level by both Georgia (GDNR 2008) and Tennessee (TDEC 2008). As suggested by its protection statuses, S. montana is usually found in low density, rarely exceeding more than a few plants per square 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 101 meter (Cruzan 2001). Forests in which S. montana occurs typically feature a relatively open, mid-to-late successional, and predominately oak-hickory or mixed-oak canopy with possible occurrences of native Pinus spp. (pine) and Vaccinium spp. (blueberry) (Cruzan 2001, Mulhouse et al. 2008, USFWS 2002). Associated soils are generally shallow, loose, rocky, well-drained, and slightly acidic (USFWS 2002; H.M. Kile, J. Shaw, and J. Nagel Boyd, pers. observ.). At the time of its federal reclassification, 48 populations of S. montana had been documented with a viable population defined as having over 100 individuals and separated by a distance of 0.8 km from another occurrence (USFWS 2002). The VTS has a large population of this species, and although S. montana individuals at the VTS are protected, at times plants may be disturbed unavoidably by necessary activities associated with the training and security directives of military operations. Such activities include complete clearing of vegetation taller than grasses and herbs along site boundaries in accordance with site security procedures and prescribed burning to reduce fuel loads to prevent and control wildfires that could be produced by training at an on-site tank-firing range and small-arms weaponry practice. Prescribed burning treatments in forested communities often increase light, soil moisture, and short-term nutrient availability to perennial herbaceous understory species (Huang et al. 2007). Consequently, to persist and perform successfully in burned conditions, these species must be able to respond positively to increased resource availability resulting from fire. A recent study conducted in a mixed-oak forest in the central Appalachian Mountains reported that understory perennial species in that community generally responded positively to prescribed burning with enhanced photosynthetic performance and productivity (Huang et al. 2007); however, the magnitude, timing, and frequency of fire regimes can be important factors to consider in elucidating the impacts of fire on plant species responses. For example, frequent low-severity fires during a dormant season may only minimally impact the understory light environment (Hutchinson et al. 2005), while severe and/or infrequent fire during a growing season could produce more dramatic changes in resource availability. Canopy thinning, which also increases light availability to the deciduous forest understory, has been associated with altered understory vegetation cover (Thomas et al. 1999). However, the magnitude and degree of such responses can be influenced by thinning intensity, vegetation life form, and compounding environmental conditions (Thomas et al. 1999). Reports of the observed responses of S. montana to burning, clearing, and associated alternations in resource availability have been limited and somewhat contradictory. Previous observation has suggested that S. montana survives prescribed burning and logging activities, but it has been speculated that recruitment after such disturbances is low (USFWS 2002). It also has been suggested that canopy disturbances resulting in greater light availability are beneficial to this species (Nix et al. 1993, USFWS 2002), but soil disturbances could negatively impact S. montana due to competition pressures (Nix et al. 1993). Furthermore, Fail and Sommers (1993) suggested that fire suppression activities may be a fac102 Southeastern Naturalist Vol. 12, No. 1 tor influencing the rarity of S. montana, yet as late as 2005, the United States Forest Service classified S. montana as adversely affected by fire (Owen and Brown 2005). Mulhouse et al. (2008) reasoned that since S. montana habitat often had a strong understory grass component, its habitat would tend to also have relatively high light availability. However, an evaluation of canopy openness at the location of S. montana individuals sampled in the Tennessee River Gorge with hemispherical photography found no correlation between percent canopy openness and growth or reproductive variables including leaf number and flower number in this species (see Hopkins 1999). To understand how operational disturbances at the VTS could influence S. montana there, we designed a field investigation to study the effects of burning and thinning treatments on S. montana transplants removed from site boundaries prior to their clearing. Our objectives were to provide recommendations for land managers at the VTS and elsewhere regarding the response of this species to transplantation and anthropogenic disturbances and to guide site selection for future transplantation when plant rescue is necessary. The individuals that were transplanted were largely adult-stage plants, which have been proposed to have higher initial survivability than seeds or seedlings (Drayton and Primack 2000, Wendelberger et al. 2008). We assessed the post-transplantation survival, growth, reproductive potential, and development, which are all early fitness indicators and are thought to be site dependent and influenced by ecological pressures (Jusaitis 2005, Menges 2008, van Andel 1998). Additionally, because photosynthetic activity in response to resource availability has been shown to positively affect plant productivity (Bazzaz 1990, Ceulemans and Mousseau 1994, Eamus and Jarvis 1989, Kimball 1983, Lawlor and Keys 1993, Mooney et al. 1991), we also investigated leaf-level gas exchange and related factors of S. montana individuals post-transplantation. Field-site Description The VTS is a 648-ha military training facility (≈34°93′N, 85°06′W) located in Catoosa County, GA (Fig. 1). In nearby Chattanooga, TN, July is the warmest month with an average high temperature of 32.2 ºC and an average low of 20.9 ºC; January is the coolest month with an average daily high temperature of 10.2 ºC and an average low of -0.6 ºC (NWS 2012). Mean annual precipitation in Chattanooga is 133.4 cm; February is the wettest month with 12.7 cm of precipitation, while October is the driest month with 8.3 cm of precipitation (NWS 2012). Mean elevation of the VTS is 250 m. Approximately 80% of the site is covered by mixed-oak forest, and several streams and gravel roads cross the property. Military installations with significant natural resources are required to draft plans for managing these resources, which should include endangered-species management guidelines, in conjunction with the USFWS and state wildlife agencies (Army 2007). The purposes of such plans are to promote sustainable use of 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 103 military lands while maintaining operational missions. The VTS was first surveyed for S. montana in 2002 at the recommendation of the USFWS, which resulted in the documentation of more than 1500 individual plants distributed in 60 clusters (SAIC 2002). These clusters were subsequently grouped into 26 management Figure 1. Location of the study site. Portions of Tennessee, Alabama, and Georgia are shown with counties outlined in light gray. The inset is of Catoosa County with the Tennessee Army National Guard Volunteer Training Site shown in dark gray. Scutellaria montana also is known to occur in the dark gray counties surrounding Catoosa County, GA. 104 Southeastern Naturalist Vol. 12, No. 1 groups based on their proximity (SAIC 2002). To monitor population trends and to determine the impacts of operational activities on S. montana, forty-six 10-mradius permanent plots were established within the VTS in 2004 (SAIC 2006). As of the last formal survey of these monitoring plots in spring 2010, the number of S. montana individuals in plots (n = 1346 plants) was greater than the average number of individuals observed in plots during growing seasons since plot establishment (mean = 1156 plants; Boyd et al. 2010). A security directive at the VTS requires vegetation clearing of a ≈7.6-m (25- ft) buffer inside the fenced property line, which would result in a drastic habitat change from forest to an open area without a canopy. During spring 2009, S. montana individuals along site boundaries in four locations were determined to be affected by vegetation clearing scheduled for 2010 because they occurred within the interior buffer of the training site. To mitigate potentially negative impacts of this disturbance, the TNARNG was required to replace three times the number of affected plants with S. montana grown from local seeds (L. Lecher, State of Tennessee Military Department, pers. comm.). Additionally, we were given permission to relocate S. montana individuals occurring along areas of the VTS boundary scheduled for vegetation clearing to a non-plot area of the VTS. We decided to utilize these individuals toward quantifying the effects of prescribed burning and canopy clearing prior to transplantation on initial transplantation success and subsequent performance in this species. Methods Pre-relocation treatments In January 2010, we selected a site for the relocation of S. montana individuals scheduled to be impacted by 2010 boundary-line vegetation clearing. The relocation site is located within one of the existing management groups of known S. montana habitat at the VTS and had no plans for development in the foreseeable future. Within the relocation site, four 35-m2 plots were established on a gentle slope of an east-facing aspect approximately 25 m below a gravel road and several meters upland from an ephemeral stream. A low-grade prescribed burning treatment was applied to two of the plots by VTS personnel in March 2010, and only the leaf litter was consumed with this treatment. In one of the burned and one of the unburned plots, woody stems less than 15-cm diameter at breast height were manually cleared, and larger woody stems were girdled. The burned area was spaced approximately 100 m from the unburned area, and the plots within each area were approximately 5 m apart. The resultant pre-relocation plot treatments consisted of control (C), burned only (B), canopy- thinned only (T), and combined burned and canopy-thinned (B+T) plots. Transplantation During the 2009 growing season, we located and flagged 100 S. montana individuals occurring within three clusters on the western boundary and one 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 105 cluster on the eastern boundary of the VTS and assigned each of these individuals randomly to a specific location within one of four pre-treated relocation plots. Therefore, plots had 25 transplants each. Because S. montana can be cespitose, all stems within 10 cm of each other were considered to be parts of an individual plant. Approximately one week prior to transplantation in spring 2010, holes were pre-dug in the relocation plots spaced 1 m apart along north–south transects. Transplantation occurred during three days in late April and early May 2010. Given the shallow soils characteristic of the site and to minimize root disturbance, an approximately 30-cm-diameter, 15-cm-deep cylinder of intact soil was carefully dug around each S. montana individual. Each plant (and its surrounding soil) was transferred quickly into a large nursery container for transport by vehicle to the relocation site during the same day. All individuals were placed in their pre-assigned specific location in the relocation plots and immediately covered with soil and any available leaf litter. Because transplantation disturbs the soil and root contact, water stress can result in dry soils before sufficient establishment takes place (Jusaitis 2005, Taiz and Zeiger 2006). To prevent this, all transplants were watered daily through the first week after transplantation and then on a weekly basis, if there was no rain, up until the end of July 2010. Post-transplantation site analyses To determine the influence of prescribed burning on soil resource availability, we collected soil samples in July 2010 at a depth of approximately 10 cm from the plot centers. These samples were homogenized and sent to the Soil, Plant, and Water Laboratory at the University of Georgia in Athens, GA for soil nutrient analysis. In August 2010, hemispherical photographs were taken according to previous methods (see Rich 1990, Zhang et al. 2005) with a digital camera mounted on a tripod from the center of each plot to determine the percent canopy openness provided by thinning treatments. Photographs were analyzed with internet- downloadable software, Gap Light Analyzer 2.0 (Simon Fraser University, Burnaby, BC, Canada, 1999). Post-transplantation measurements Surveys to monitor transplanted S. montana individuals were conducted throughout the 2010 and 2011 growing seasons. Reported inventories were conducted on 7 May 2010, 27 May 2010 for flowering, 20 May 2011, and both 10 August 2010 and 15 July 2011 for transplant survival. Survival was expressed as transplants with existing aboveground biomass as a percentage of the total transplants at the beginning. Baseline metrics for growth included stem height (of the tallest stem in multiple-stemmed individuals), the number of stems, and the number of leaves of each individual plant. Reproductive potential and development were assessed by determining the developmental stage classes of all individuals and counting the numbers of flowers per 106 Southeastern Naturalist Vol. 12, No. 1 individual. We defined stage classes as juvenile for plants with stem height <10 cm and not showing any thickened bases (a clear indication that they had been damaged, e.g., by vertebrate browsing), vegetative adult for plants with stem height >10 cm, and flowering adult for plant bearing flowers or fruits. Additionally, we noted damage during all inventories including irregular patterns of leaf biomass removal as could be caused by herbivores and stem damage, which was largely assumed to result from vertebrate grazing, especially when apical biomass was found missing, although stems were occasionally found bent or broken after heavy rains, or possibly from vertebrate trampling. To elucidate the physiological mechanisms underlying growth, reproductive, and developmental observations, we measured instantaneous leaf-level gas exchange with a portable gas-exchange analyzer (LI-6400XT, LI-COR, Lincoln, NE) on 21 July 2010. All plants were watered in the morning prior to gas-exchange measurements. A clear-top leaf cuvette was used to provide ambient light conditions during measurements, and conditions within the cuvette were set to mimic ambient conditions of 400 μmol CO2 mol-1 and 29 ºC temperature. Gasexchange measurements included net photosynthetic rate (A; μmol CO2 m-2 s-1), as well as transpiration rate (E; mol H2O m-2 s-1) and stomatal conductance (gs; mol H2O m-2 s-1) expressed per unit leaf area. Additionally, small subsamples of leaf biomass were collected immediately following gas-exchange measurements and dried to calculate the leaf mass per unit area (LMA), which is generally correlated with leaf-level photosynthetic activity (Field and Mooney 1986; Reich et al. 1991, 1992, 1997). Statistical analyses A two-way analysis of variance (ANOVA) was conducted to evaluate the main effects and interactive effect of burning and canopy-thinning treatments on measured variables. Main and interactive effects of treatments were considered significant if P ≤ 0.05. Principal component analysis (PCA) with an orthogonal rotation was used to test relationships between variables. All statistical analyses were performed with IBM SPSS Statistics 19 (SPSS, Inc., 2010, S omer, NY). Results Plot treatments Burning had a positive influence on the availability of select soil nutrients. In comparison with control plot C, plot B was characterized by 26% greater ammonium (NH4 +) availability and 67% greater potassium (K) availability (Table 1). In addition, soil K was 75% greater and nitrate (NO3 -) was 33.3% greater in plot B+T than in plot C (Table 1). With the exception of NO3 -, differences in soil nutrient availability between plots T and C were more minimal than differences between plots B and C (Table 1). Overall, canopy thinning increased the openness of relocation plots. Specifically, percent canopy openness was 10.4% in plot C, 13.5% in plot B, 20.8% in plot T, and 18.7% in plot B+T. 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 107 Overall transplant survival, growth, and reproduction When baseline metrics were assessed less than one week after transplantation was complete, two transplanted S. montana individuals were missing from their relocation positions. During the 2010 growing season, four individuals senesced; two of these plants appeared to have experienced mechanical basal damage, while the other two individuals exhibited no apparent reasons for sensescence. Two senesced individuals grew new shoots within a few weeks, while the other two individuals regenerated during the next year. Including senesced individuals, 98% of transplanted S. montana individuals survived to our August 2010 inventory. During the May 2011 inventory, 12 plants were not found in their relocation positions (including the two individuals missing during our May 2010 inventory). However, three of these individuals produced aboveground biomass by our July 2011 inventory, resulting in 91% survival of original transplants by late into the second growing season after being relocated. During our May 2010 baseline measurements, we found that S. montana transplants across all relocation plots were mostly single-stemmed, but the number of stems per individual plant ranged from 1–3. Individual plant stem height ranged from 2.5–45 cm, and the number of leaves per plant ranged from 2–16 (Table 2). In addition, leaf damage was observed on 58% of the total transplanted S. montana individuals, while stem damage was observed on 14% of transplants. Across all relocation plots, 27% of transplants were juveniles, 51% were vegetative adults, and 22% were reproductive (i.e., flowering or fruiting) adults. A total of 50 flowers were counted for all transplants. Table 1. Amount (mg/kg) of soil ammonium (NH4+), nitrate (NO3-), phosphorus (P) and potassium (K) in control (C), burned only (B), thinned only (T), and burned and thinned (B + T) Scutellaria montana relocation plots at the Tennessee Army National Guard Volunteer Training Site in Catoosa County, GA. Relocation plots Soil nutrients (mg/kg) C B T B+T NH4 + 8.8 11.1 9.8 9.7 NO3 - 0.8 1.7 1.7 3.3 P 10.5 11.8 8.9 9.5 K 68.8 115.0 76.5 120.5 Table 2. Mean (± SE) values of growth variables of Scutellaria montana individuals approximately two weeks (May 2010) and one year (May 2011) post-transplantation across relocation plots at the Tennessee Army National Guard Volunteer Training Site in Catoosa County, GA. Survey date Variable May 2010 (n = 98) May 2011 (n = 88) Number of stems 1.1 ± 0.38 1.7 ± 0.10 Stem height (cm) 12.0 ± 8.1 20.0 ± 1.1 Number of leaves 6.8 ± 2.7 21.2 ± 1.6 Number of flowers 0.5 ± 1.5 3.3 ± 0.6 108 Southeastern Naturalist Vol. 12, No. 1 By approximately one year post-transplantation, the upper ranges of growth measurements were greater than during baseline measurements. Specifically, the number of stems per plant ranged from 1–5, stem height ranged from 1–54.5 cm, and the numbers of leaves per plant ranged from 0–78 across all relocated plots in May 2011 (Table 2). However, damage to both leaves and stems also increased from 2010 to 2011. Leaf damage was observed on 67% of the total transplanted S. montana individuals, while 57% of transplants exhibited stem damage in May 2011. In addition, the transplants included 5.7% juveniles, 56.8% vegetative adults, and 37.5% flowering adults in May 2011, and a total of 293 flowers were counted at that time, evidencing that the transplanted individuals as a group were aging. Our PCA of measured growth factors (stem height, and stem, leaf, and flower number per individual plant) revealed that two components explained 87.3% of the variation in growth exhibited by the transplants (Table 3). Stem number of S. montana individuals was strongly and positively associated with leaf number, while stem height was strongly and positively associated with flower number (Fig. 2). Responses of transplants to burning and thinning When compared with survival in control plot C, the percent of S. montana transplants that survived to July 2011 was greater with burning alone, but lower when the relocation area was subjected to canopy thinning. Transplant survival was 96% in the plot C, 100% in plot B, and 84% in both plot T and plot B+T. In May 2010, there were no significant differences in any of the measured growth, reproductive, and developmental variables or observed biomass damage of S. montana transplants between relocation plots (all P > 0.10); however, significant differences in several of these variables was exhibited in May 2011. These differences included both main and interactive effects of burning and canopy thinning. Specifically, burning negatively influenced both the proportion of plants with leaf damage (P < 0.001, F3,87 = 14.322; Fig. 3a) and the proportion of plants that were flowering adults (P = 0.003, F3,87 = 9.036; Fig. 3b), while the proportion of plants exhibiting stem damage (P = 0.030, F3,87 = 4.845; Fig. 3c) and the proportion of plants that were vegetative adults Table 3. Varimax-rotated matrix of a principle component analysis (PCA) showing the variable loading per component, total eigenvalue, and cumulative variance explained (%) in growth variables measured for Scutellaria montana in May 2011 at the Tennessee Army National Guard Volunteer Training Site in Catoosa County, GA. Component Variable 1 2 Number of stems 0.973 Stem height (cm) 0.880 Number of leaves 0.468 0.837 Number of flowers 0.903 Total eigenvalue 1.81 1.68 Cumulative variance explained (%) 45.3 42.0 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 109 (P = 0.009, F3,87 = 7.242; Fig. 3d) were positively influenced by burning. However, burning did not influence significantly the mean stem height (P = 0.254) per transplanted S. montana individual, the mean number of stems (P = 0.819), leaves (P = 0.277), or flowers (P = 0.099) of transplants, or the proportion of transplants that were juveniles (P = 0.714). Canopy thinning negatively influenced both mean stem height per individual (P = 0.009; F3,87 = 7.107; Fig. 4a) and the proportion of plants that were flowering adults (P = 0.009, F3,87 = 7.075; Fig. 4b), while both the proportion of plants exhibiting stem damage (P = 0.001, F3,87 = 10.838; Fig. 4c) and the number of vegetative adults responded positively to canopy thinning (P = 0.025, F3,87 = 5.185; Fig. 4d). In contrast, canopy thinning did not influence significantly the number of stems (P = 0.074), leaves (P = 0.926) and flowers (P = 0.083) per individual transplant, the proportion of plants with leaf damage (P = 0.123), or proportion of plants that were juveniles (P = 0.595). Interactive effects of burning and canopy thinning on S. montana growth, reproductive potential, development, and biomass damage were more limited than the main effects of either treatment. Only mean stem height (P = 0.004, F3,87 = Figure 2. Principal component analysis (PCA) projection of stem height, and numbers of stems, leaves, and flowers of transplanted Scutellaria montana individuals in May 2011 at the Tennessee Army National Guard Volunteer Training Site in Catoosa County, GA. Percentages of the two components represent total variance explained, and projections in the same direction show positive correlations, while opposite directions would have represented negative correlations. 110 Southeastern Naturalist Vol. 12, No. 1 8.844) and the number of leaves per S. montana transplant (P = 0.015, F3,87 = 6.151) were influenced significantly by the interaction of burning and canopy thinning. Specifically, burning negatively influenced both the mean stem height and number of leaves per transplanted S. montana individual when combined with canopy thinning but positively influenced stem height in unthinned plots relative to the absence of burning (Fig. 5). Leaf-level gas exchange and related factors of S. montana transplants exhibited some shared responses to the main effects of burning and canopy thinning. Specifically, transplants in burned plots were characterized by significantly greater LMA than those in unburned plots (P < 0.001, F3,76 = 55.223; Fig. 6a), while transplants in thinned plots were characterized by significantly greater LMA than those in unthinned plots (P < 0.001, F3,76 = 27.526; Fig. 6b). Similarly, transplants in burned plots were characterized by significantly greater E than those in unburned plots (P = 0.007, F3,60 = 7.710; Fig. 6c), while transplants in thinned plots were characterized by significantly greater E than those in unthinned plots (P = 0.004, F3,60 = 8.919; Fig. 6d). Burning also was associated with a significant increase in leaf A (P = 0.045, F3,60 = 4.191; Fig. 6e), while canopy thinning also was associated with a significant increase in leaf gs (P = 0.011, Figure 3. The significant main effect (P ≤ 0.05) of burning on the proportion of plants with leaf damage (a; % of total), the proportion of plants that were flowering adults (b; % of total), the proportion of plants with stem damage (c; % of total), and the proportion of plants that were vegetative adults (d; % of total) of transplanted Scutellaria montana individuals at the Tennessee Army National Guard Volunteer Training Site in Catoosa, GA. Values shown on means ± 1 SE. 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 111 Figure 4. The significant main effect (P ≤ 0.05) of thinning on the stem height (a; cm), the proportion of plants that were flowering adults (b; % of total), the proportion of plants with stem damage (c; % of total), and the proportion of plants that were vegetative adults (d; % of total) of transplanted Scutellaria montana individuals at the Tennessee Army National Guard Volunteer Training Site in Catoosa, GA. Values shown on means ± 1 SE. F3,60 = 6.824; Fig. 6f). In contrast, leaf gs did not differ significantly between burned and unburned plots (P = 0.078), while leaf A did not differ significantly between thinned and unthinned plots ( P = 0.229). Figure 5. The significant interaction effect (P ≤ 0.05) of burning and canopy thinning on mean stem height (a; cm) and the number of leaves per individual (b) of transplanted Scutellaria montana at the Tennessee Army National Guard Volunteer Training Site in Catoosa, GA. 112 Southeastern Naturalist Vol. 12, No. 1 Discussion Transplantation as mitigation Overall, we consider our S. montana transplantation efforts to be successful because transplants exhibited high survival, maturation in terms of both individual growth and collective development, and increased reproductive potential as evidenced by total flower production one year after their relocation (Table 2). However, seedlings were not observed concurrently, so we cannot yet determine if the transplants will comprise a self-sustaining group. In general, the transplantation of rare plant species often has been associated with less-than-ideal long-term results due to inherent life-history traits, such as low seed set and recruitment (Fahselt 2007). Figure 6. The significant main effect (P ≤ 0.05) of burning on leaf mass per unit area (a; LMA in g m-2), instantaneous leaf-level transpiration rate (b; E in mol H2O m-2 s-1), and instantaneous leaf-level photosynthetic rate (c; A in μmol CO2 m-2 s-1), and the significant main effect (P ≤ 0.05) of thinning on LMA (d), E (e), and instantaneous stomatal conductance (f; gs in mol H2O m-2 s-1) of transplanted Scutellaria montana individuals at the Tennessee Army National Guard Volunteer Training Site in Catoosa, GA. Values shown on means ± 1 SE. 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 113 Seedling survival, in particular, has been identified as one of the most significant barriers to self-sustenance in transplanted populations, especially for at-risk species (Jusaitis 2005, Lofflin and Kephart 2005), and recruitment is influenced by both seed availability and favorable environmental conditions for seedling establishment (Eriksson and Ehrlen 1992). Previous observations of S. montana have suggested that this species is characterized by limited flowering, fruit set, and seed set in natural conditions (Cruzan 2001, Hopkins 1999, Kemp 1987, Nix et al. 1993, USFWS 2002). However, because flower number has been associated positively with fruit set in this species (Hopkins 1999), the increased number of flowers we found one-year post-transplantation in our study could be indicative of future increased seed availability. Yet, the establishment of any future seeds could be impacted negatively by abiotic and biotic factors such as summer droughts (Manzaneda et al. 2005), herbivory, and competition from neighboring vegetation (Jusaitis 2005). Continued monitoring of S. montana transplants and surveys of the relocation plots utilized in this study for recruits will be important for evaluating the longer-term success of our efforts. Importance of site selection Despite previous suggestions that S. montana habitat may be characterized by relatively high light availability within the forest understory (Mulhouse et al. 2008) and that canopy disturbances resulting in greater light availability are beneficial to this species (Nix et al. 1993, USFWS 2002), we found that transplant survival was reduced in thinned relocation plots in comparison to plots with intact canopy. Furthermore, S. montana in thinned plots were comparatively shorter in stature, had more stem damage, and exhibited less reproductive potential than in unthinned plots (Fig. 4). We suggest that the concurrent increases in leaf LMA, E, and gs that we observed for S. montana in thinned plots compared with unthinned plots are indicative of leaf acclimation to increased light availability (Chabot et al. 1979; Fig. 6). The positive association of light availability with LMA, in particular, is considered an ecological adaptation that increases leaf surface area for greater light interception in low-light conditions and reflects the greater incorporation of photosynthetic enzymes and machinery in leaves under high-light conditions (Poorter et al. 2009). Although such leaf-level factors theoretically could reflect an increased capacity for energy assimilation, we did not observe any concurrent positive responses of growth or development of S. montana with increased light availability provided by canopy thinning. As such, our results suggest that canopy thinning does not benefit, and could negatively impact, the success of S. montana transplantation efforts. In contrast to the effects of canopy thinning, we found that S. montana transplant survival in this study was minimally enhanced by burning (in the absence of thinning) in comparison to a lack of burning. Although it has been suggested previously that S. montana responds poorly to fire (Owen and Brown 2005, USFWS 2002), these suggestions were based largely on the 114 Southeastern Naturalist Vol. 12, No. 1 survival of existent plants to burning rather than the use of burning as a pretreatment for future transplants. However, while burning influenced survival positively in our study, burning also was associated with greater stem damage and reduced reproductive potential among S. montana transplants than observed in unburned plots (Fig. 3). Burning also had a negative impact on both stem height and the number of leaves produced per S. montana individual when combined with canopy thinning (Fig. 5). As with canopy thinning, we suggest that the increased leaf LMA, E, and A exhibited by S. montana individuals in burned plots compared with unburned plots could reflect leaf acclimation to increased light availability to some extent given the effect of our low-grade burning treatment on the density of surrounding understory vegetation (Fig. 6). We also suggest such acclimation could have been influenced by greater availability of soil N in burned compared with unburned plots (Table 1) since N is incorporated into photosynthetic enzymes. While we did not measure foliar nitrogen (N) in this study, this factor typically is positively correlated with increased photosynthetic capacity (Evans 1989, Frak et al. 2001, Niinemets 1999, Reich et al. 1997). Additionally, positive correlations between foliar N content and gas exchange have previously been evidenced in plant responses to prescribed burning treatments, and E, in particular, was increased at all times of the day (Reich et al. 1990). However, as with canopy thinning, we did not observe any concurrent positive responses of growth or development of S. montana with burning alone, suggesting that leaf-level changes had limited influence on whole-plant processes within this species and the scope of our study. Given the negative impacts of burning on S. montana stem damage and transplant development observed in this study, we conclude that burning could negatively impact the success of S. montana transplantation efforts. However, because Native Americans are thought to have greatly influenced the Ridge and Valley physiographic providence with fire before Europeans settlers arrived (Delcourt and Delcourt 1998), we suggest that further investigations of the fire adaptability of S. montana, including investigation of the effects of burning on seed germination, recruitment, and interspecific competition of surrounding postfire vegetation, are warranted. Possible impact of herbivores The increased stem damage of S. montana that we observed with transplantation and in response to burning and canopy thinning indicate that herbivores may have been especially attracted to our relocation plots. Across treatments, the 3.6-fold increase in stem damage that we observed one year post-transplantation was unexpected. Naturally occurring S. montana individuals sampled across the VTS in May 2010 (n = 1346) exhibited 8% stem damage, while individuals within the two permanent monitoring plots closest in proximity to the relocation plots exhibited 12% (n = 150) and 19% (n = 26) stem damage (Boyd et al. 2010). The similarity of stem damage in plot C (27%) to those monitoring plots suggests that overall stem damage among transplants 2013 H.M. Kile, J. Shaw, and J. Nagel Boyd 115 was influenced greatly by the very positive impact of burning and canopy thinning on this factor (Figs. 3, 4). Furthermore, we suggest that increased herbivory in burned and thinning plots could have skewed our site-selection analysis regarding the influence of these treatments on the success of S. montana transplantation. Specifically, stem damage typically was observed as missing apical portions of biomass; inherently, this would decrease stem height. Because S. montana has a terminal inflorescence, we also suggest that flowers may have been produced and subsequently consumed by grazers prior to survey times, which could have reduced our flower counts and affected our assessments of flowering adults. Hopkins (1999) reported a positive relationship of the number of leaves with the number of flowers per individual of S. montana, but our PCA suggested that stem height was a better indicator of flower number in the transplants than leaf number, lending further support to our hypothesis that flower counts were influenced by grazing in this study (Fig. 2). Comparison with previous transplantation efforts Previous attempts at transplantation of S. montana have had mixed results (Snyder and Lecher 2010, McKerrow 1996, USFWS 2002). However, high initial survivability was found after our transplantation of S. montana at a nearby site prior to our implementation of this study (Kile et al. 2011). Specifically, we transplanted 49 S. montana individuals in May 2009 from a small location in the Enterprise South Nature Park in Chattanooga, TN, that was scheduled to be impacted by highway construction project to a nearby area with existing S. montana individuals, as recommended by the USFWS. One month after this relocation, an ≈1.25-m-tall chain-link fence was constructed around the relocation site to exclude human traffic given its close proximity to a road and hiking and biking trails. Overall, survival of these plants was very high (98%) one year post-transplantation, similar to our VTS transplants. Our Enterprise South transplants experienced an approximate 190% increase in stem height, 45% increase in the number of stems per individual, 130% increase in the number of leaves per individual, and 2000% increase in the number of flowers per individual one year post-transplantation (Kile et al. 2011). In contrast, the VTS transplants experienced a 67% increase in stem height, 55% increase in the number of stems per individual, 212% increase in the number of leaves per individual, and 547% increase in the number of flowers per individual (Table 2) one year post-transplantation. The Enterprise South transplants also experienced a 93% reduction in the proportion of plants with stem damage one year post-transplantation, in contrast to the increase in stem damage observed for the VTS transplants after this same duration. Combined, these comparisons suggest that protection of S. montana transplants from herbivores could maximize their success and allow for better elucidation of the influence of disturbances like burning and thinning on transplantation success. 116 Southeastern Naturalist Vol. 12, No. 1 Conclusions Our overall S. montana transplantation results evidenced initial success with high survivability, continued maturity, and increased reproductive effort. However, both burning and canopy thinning were associated with reduced transplant development and reproductive potential, increased stem damage, and likely increased associated herbivory compared with a lack of these treatments. As such, we recommend that future relocation sites include locations with known S. montana occurrences and avoid areas recently disturbed by burning or canopy thinning unless plans are made for the subsequent control of vertebrate herbivory. More broadly, we suggest that herbivore exclosures be utilized for all S. montana transplants to maximize their post-transplantation success. Additionally, we suggest that the S. montana transplants described in this study continue to be monitored, and that future monitoring include a search for new recruits to determine if transplants will be self-sustaining. Because human activities have an ongoing environmental impact at many scales, effective plant species conservation and management should benefit from increased understanding of the effects of such activities on these species. Ultimately, the findings of this study should aid efforts to protect and support S. montana in the VTS and other locations impacted by necessary human disturbance, as well as provide insight into the potential influence of such disturbances on other endangered, threatened, and/or rare herbaceous plant species of the deciduous forest understory. Acknowledgments We acknowledge the Tennessee Army National Guard for providing the primary funding for this project. We thank Laura Lecher of the State of Tennessee Military Department and Sgt. Todd Anderson and his staff at the Tennessee Army National Guard Volunteer Training Site for their assistance and cooperation in accommodating and providing logistical support for our research. 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