Northeastern Naturalist Vol. 24, No. 2 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 191 2017 NORTHEASTERN NATURALIST 24(2):191–200 Differential Responses to Light and Nutrient Availability by Geographically Isolated Poison Ivy Accessions John G. Jelesko1, Elise B. Benhase2, and Jacob N. Barney1,* Abstract - The morphology and growth habit of Toxicodendron radicans (Poison Ivy) varies widely across North America. In this study, we evaluated the role of Poison Ivy accessionlevel diversity on growth habit and performance responses to light and nutrient stress in a common-garden greenhouse environment. We grew Poison Ivy seedlings derived from drupes collected from Iowa (IA), Michigan (MI), Texas (TX), and Virginia (VA) in a glasshouse with factorial arrangements of 2 light treatments (full sun and deep shade) and 3 nutrient treatments (full nutrients, full nutrients minus nitrogen, no nutrients). Seedlings from Iowa grew very poorly across all treatments, whereas plants from MI, TX, and VA showed accessional variation, though treatment effects were stronger than accession-level effects. We observed significant accession-level differences in height, branch number, leaf area, total biomass, chlorophyll, and root:shoot ratio biometrics; the Texas accession generally outperformed the MI and VA accessions across all treatments. Overall, light availability was a much stronger driver of overall performance than nutrient availability; plants grown in shade were smaller, had fewer branches and produced ~20% of the biomass compared to those grown in full-sun. Poison Ivy shows accession-level variation in plastic responses to light and nutrient availability, which partially explains the breadth of habitats the species colonizes. Introduction Toxicodendron radicans (L.) Kuntze (Poison Ivy) is a common native liana found throughout eastern US forests, urban areas, and disturbed sites (Kuntze 1891). Human contact with any portion of plants of this species results in delayed allergenic dermatitis symptoms in about 80% of the population (Epstein 1987). The natural compound responsible for these clinical symptoms is generically called urushiol (ElSohly et al. 1986, Johnson et al. 1972). In contrast, deer, squirrels, and goats readily eat Poison Ivy foliage without any demonstrable ill effects (Martin et al. 1951, Penner et al. 1999, Popay and Field 1996, Senchina 2008). Similarly, a number of bird species eat Poison Ivy drupes without any apparent harm (Martin et al. 1951, Penner et al. 1999, Suthers et al. 2000). Thus, the presence of urushiol in nearly all plant parts suggests an important ecological function that remains enigmatic. Poison Ivy shows a very high degree of anatomical polymorphism across North America. For many years, Poison Ivy was classified as a member of the Rhus genus that included both allergenic contact-dermatitis–causing species, and those that do not (Barkley 1937). However, in a 1971 monograph, William Gillis moved all 1Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, VA 24061-0331. 2Lewis Ginter Botanical Garden, 1800 Lakeside Avenue, Richmond, VA 23228. *Corresponding author - jnbarney@vt.edu. Manuscript Editor: Douglas DeBerry Northeastern Naturalist 192 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 Vol. 24, No. 2 allergenic Rhus members into the unified genus Toxicodendron, and extensively described Poison Ivy and Toxicodendron diversilobum (Torr. & A. Gray) Greene (Poison Oak) biogeography (Gillis 1971). He assigned 4 major species within the genus: Toxicodendron diversilobum (Torr. & A. Gray) Greene (Western Poison Oak), T. toxicarium (Salisb.) (Eastern Poison Oak), T. rydbergii (Small ex Rydb.) Greene (Western Poison Ivy), and T. radicans (Poison Ivy). Based upon both biogeography and a variety of traits, Gillis further subdivided T. radicans into a number of subspecies: barkleyi, divaricatum, eximium, hispidum, negundo, pubens, radicans, and verrucosum. Gillis also described apparent intergrade zones with presumed hybrids showing intermediate traits. The latter suggests localized genetic adaption of isolated Poison Ivy populations. Poison Ivy is often purported to be associated with edge habitats, particularly those formed by managed lands. Upon closer examination, these assertions seem to be derived from anecdotal observations, rather than systematic investigations. Gillis examined the Baker Woodlot in East Lansing, MI, for expected preferential T. radicans ssp. negundo (Greene) growth at the edges of the woodland; however, he concluded that light availability alone could not account for the observed patterns of Poison Ivy presence and absence at the woodland edges (Gillis 1971). Gillis speculated that the natural range of poison ivy and poison oak species may have dramatically expanded in response to historical European immigrant land-management patterns. For example, records from Spanish colonization of California during the 16th and 17th centuries did not mention allergenic poison oak as a native plant species, suggesting it was relatively rare during this period. In contrast, Western Poison Oak is a widespread and common weedy species in California today. Poison Ivy is adapted to exploit a variety of habitats because it can grow as a shrub, creeping stolon, and/or a liana (Gillis 1971), suggesting high phenotypic plasticity. In contrast, Western Poison Ivy diplays only shrub and creeping-stolon growth habits. The multiplicity of poison ivy growth-habit capacity enables it to rapidly respond to both natural (Allen et al. 1997, Allen 2005) and anthropogenic disturbances (Catling et al. 2002, Gillis 1971). The species’ adaptive traits include rapid growth rate with accompanying accumulation of biomass and shifting urushiol congener levels to more-allergenic urushiol-congener composition in response to elevated CO2 (Mohan et al. 2006, Ziska et al. 2007). Despite the widespread incidence of poison ivy in North America, its ecology is poorly understood, particularly regarding performance responses to common environmental stressors. With the anticipation of increased land-use change and continued habitat fragmentation, an understanding of how Poison Ivy responds to environmental variation will aid characterization of how this native invader will respond to further anthropogenic changes. Therefore, our objective was to determine if Poison Ivy exhibits intra-specific variation in response to light and nutrient availability. Materials and Methods We evaluated accession-level variation in stress response by 4 Poison Ivy plants representing a wide geographical distribution: Roanoke County, VA (37°22'52.5"N, Northeastern Naturalist Vol. 24, No. 2 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 193 80°06'39.2"W), collected in August 2012; Basrop County, TX (30°104.5588"N, 97°24'11.019"W), collected in September 2012; Dallas County, IA (New York Botanical Garden herbarium barcode 02111147; 41°39'26.4954"N, 94°0'27.9714" W), collected in September 2013; and Ingram County, MI (42°45'7.8696"N, 84°35'7.8684"W) collected in October 2013. No herbarium samples were prepared from the original female IA, MI, and VA lianas at the time the drupes were collected. Instead we prepared herbarium samples from seedlings generated from seeds removed from IA, MI, and VA drupes, and we deposited vouchers in the Virginia Tech Herbarium (specimen #109163, #109162, #109165, respectively). A Texas seedling-vouchered specimen #109164 was also submitted to the Virginia Tech Herbarium. We did not identify the 4 lianas to subspecies. We stored drupes in paper bags at room temperature until the experiment began. In March 2014, we mechanically and chemically scarified (Benhase and Jelesko 2013) and planted in soilless Metro-Mix media (Sun Gro, Agawam, MA) all seeds; seedlings were grown under ambient conditions in a ventilated glasshouse located at the Virginia Tech Glade Road Research facility in Blacksburg, VA. Germinating seeds were kept moist with overhead irrigation and given no additional nutrients. Three weeks after germination, we transferred the Poison Ivy seedlings to 184-cm3 square pots containing leached Metro-Mix media and kept the growing medium moist. Two of the most common abiotic environmental stressors are light and nutrient limitations. Therefore, we employed a factorial design to examine 2 levels of light availability and 3 levels of nutrient availability. On 28 April 2014, we randomly assigned seedlings to either full sun or shade environments, which were implemented as split blocks with greenhouse benches serving as whole blocks. We constructed shade environments to mimic light environments of a typical deciduous forest understory of ~10% of ambient light, which was achieved by placing plants under shade cloth supported by PVC frames. Poison Ivy is often found climbing on adjacent supports (e.g., trees); thus, we trained the primary stem of each seedling around a bamboo stake placed in the center of the pot throughout the experiment. We watered the seedlings in sufficient quantity that water was non-limiting throughout the experiment. We imposed 3 nutrient treatments within each light environment sub-plot: (1) no additional nutrients (control), (2) full macro- and micro-nutrient solution (full + N), and (3) full macro- and micro-nutrients minus nitrogen (full - N). The nutrient treatments were applied as full Hoagland solution (Hoagland and Arnon 1950) (full + N) or a Hoagland without nitrogen (full - N) and delivered as 100 ml to each pot twice a week. We established 4 whole blocks, with each block containing both light treatments, and 2 replications of each accession in each nutrient treatment. Therefore, there were a total of 48 individuals per accession (2 reps x 3 nutrient treatments x 2 light environments x 4 blocks). During the course of the experiment, we recorded the following growth and performance metrics bi-monthly: height, branch number, leaf number, and chlorophyll-content proxy using the Opti-Sciences, CCM-300 (Hudson, NH). In September 2014, after 20 weeks of growth under the experimental conditions, we Northeastern Naturalist 194 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 Vol. 24, No. 2 determined biomass by harvesting leaves, stems, branches, and roots from each seedling and then weighing the samples after they had dried at 70 °C for 1 week until mass was constant. Before drying, we used a LI-3100 Area Meter (LI-COR Environmental, Lincoln, NE) to determine total leaf area for each individual. We employed ANOVA to assess our data and considered final height (cm), leaf and branch number, chlorophyll content (mg m-2), leaf area (cm2), specific leaf area (cm2 g-1), total biomass (g), and root-to-shoot biomass ratio as response variables and Poison Ivy accession, light environment, and nutrient treatment as fixed effects. Higher-order interactions were backward-stepwise removed to improve model fit. Response variables were transformed as necessary to meet assumptions of normality of residuals and equal variance. Height, leaf area, and biomass were log10 transformed, and specific leaf area and root:shoot ratio were square-root transformed. All statistical analyses were performed in SAS JMP version 12 (Martin- Rodrigues 2013). Results Seeds from all 4 geographically isolated Poison Ivy accessions readily germinated after mechanical and chemical scarification. Seedlings from the Michigan, Texas, and Virginia accessions produced a first true-leaf pair and subsequent alternate true leaves. In contrast, the Iowa seedlings grew extremely poorly across all treatments, all individuals produced relatively few true leaves, and never progressed beyond that small growth-stage in any treatment throughout the remainder of the experiment. We did not include data from the Iowa accession in the statistical analyses because the growth habit of these seedlings was dramatically different from the other 3 accessions. The Texas, Michigan, and Virginia Poison Ivy accessions performed consistently for most traits among treatments. There were significant accession-level effects on Poison Ivy plant height (P < 0.0001), leaf area (P < 0.0001), root:shoot biomass ratio (P < 0.0001; Fig. 1b), total biomass (P < 0.0001), and chlorophyll levels (P = 0.0122) (Table 1). We observed significant light-environment effects for all parameters, except chlorophyll content (Table 1). We found significant effects in Poison Ivy response to the light environment for plant height (P = 0.0003), branch number (P < 0.0001; Fig. 2c), leaf area (P < 0.0001), specific leaf-area (P < 0.0001, Fig. 1c), root:shoot biomass (P = 0.0225), and total biomass (P < 0.0001). Significant interactions between accession and light environment were only observed for leaf area and plant height (Table 1); the Texas accession was consistently taller than the Virginia and Michigan accessions (Fig. 2a). Nutrient availability also affected Poison Ivy biometrics (Table 1). Branch number (P < 0.0001), leaf area (P < 0.0001), total biomass (P < 0.0001), and chlorophyll content (P = 0.0024) were all strongly affected by the nutrient content. The greatest effect appeared to be in response to nitrogen availability, rather than mineral micronutrients (Fig. 2d). Nutrient availability interacted strongly with the light environment for leaf area (P < 0.0001), total biomass (P < 0.0001; Fig. 1a), chlorophyll content (P < 0.0497; Fig. 2b), and weakly interacted for plant height Northeastern Naturalist Vol. 24, No. 2 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 195 (P < 0.0766). Interaction between nutrient availability and accession-level effects was limited to a weak interaction with chlorophyll content (P < 0.0841). Table 1. Statistical model P-values for performance metrics assessed at the end of the experiment. We used backwards step-wise regression to improve model fit. Model parameters with a dash (-) were not included in the model for that metric. A = accession, L = light environment, and N = nutrient availability. Leaf Specific Root/ Total Height Branch # area leaf area shoot biomass Chlorophyll A less than 0.0001 0.7297 less than 0.0001 0.2162 less than 0.0001 less than 0.0001 0.0122 L 0.0003 less than 0.0001 less than 0.0001 less than 0.0001 0.0225 less than 0.0001 0.9772 A*L 0.0245 - 0.0428 - - - - N 0.1331 less than 0.0001 less than 0.0001 0.3611 0.2157 less than 0.0001 0.0024 A*N - - - - - - 0.0841 L*N 0.0766 - less than 0.0001 - - less than 0.0001 0.0497 A*L*N - - - - - - - Figure 1. Treatment differences for Poison Ivy (a) total biomass as a function of nutrient treatment and light environment,( b) root-to-shoot ratio as a function of accession, and (c) specific leaf area as a function of light environment. See Table 1 for statistical analyses. Northeastern Naturalist 196 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 Vol. 24, No. 2 Discussion Poison Ivy is a disturbance-adapted native liana that appears to quickly colonize areas affected by both natural and anthropogenic disturbance. In 1989, hurricane Hugo caused extensive storm damage to an old-growth forest in South Carolina, resulting in widespread localized opening of the forest canopy due to downed trees. The destruction of many large trees and their associated Poison Ivy lianas, resulted in an initial decrease in Poison Ivy incidence (Allen et al. 1997). However, within 12 years Poison Ivy reestablished to higher incidence levels than before hurricane Hugo (Allen et al. 2005). This situation suggests that Poison Ivy was likely light limited. Here, we show that Poison Ivy growth (height and biomass) was significantly greater in full light compared to shade. Poison Ivy also responded favorably to nutrient additions; nitrogen was the strongest limiting nutrient. Both responses Figure 2. Treatment differences for Poison Ivy (a) height as a function of accession and light environment, (b) leaf chlorophyll content [UNITS?] as a function of light environment and nutrient treatment, (c) branch number as a function of light environment, and (d) branch number as a function of nutrient treatment. See Table 1 for statistical analyses. Northeastern Naturalist Vol. 24, No. 2 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 197 are consistent with vigorous growth following habitat disturbances that increase exposure to direct sunlight and reduce resource competition. Interestingly, we observed that 4 Poison Ivy accessions collected from across its US distribution varied in their response to stress. Fire (either natural or anthropogenic) is another type of habitat disturbance that increases both light and mineral-nutrient availability (Kutiel and Shaviv 1992). Poison Ivy incidence is positively associated with small fires in forest environments (Catling 2002). Similarly, Eastern Poison Oak is more prevalent in areas subjected to recurrent small fires (Gillis 1971); however, the exact environmental component responsible for the positive association with these burned environments was not identified. Gillis (1971) noted that Poison Ivy generally favors nutrient-rich soils with adequate drainage. The Gillis monograph summarized results from hydroponic experiments with Poison Ivy in which either iron or nitrate deficiency resulted in chlorosis, and calcium was critical for poison ivy growth and viability. In our study, the Michigan, Texas, and Virginia Poison Ivy accessions showed significant increases in total biomass and branching in response to nitrogen (full + N vs. full-N treatments); total biomass also increased in response to other mineral nutrients (full - N vs. control treatment). Interestingly, we found that Poison Ivy performance was notably enhanced when nitrogen was available in the full-sun environment, while biomass production was similar in the shade among all nutrient treatments. Leaf-chlorophyll content was higher in full-sun plants, but only in nitrogen-fertilized plants; leafchlorophyll content was lower in full sun than shade when all nutrients but nitrogen were supplied. The shade stress was not magnified by low nutrient-availability as expected; rather low light-availability reduced overall biomass production, which was not enhanced by nitrogen application. Disturbance is often associated with an increase in resource availability (e.g., nutrients, light), which is known to increase susceptibility to invasion (Davis et al. 2000). From our results, we predict that, following common forest disturbances that result in canopy gaps or opening of forest interiors, Poison Ivy will be particularly well suited to capitalizing on both light and nutrient availability. Current and future poison ivy invasiveness may continue to be enhanced as a result of an “anthropogenically induced adaptation to invade” (Hufbauer et al. 2012). There is a remarkable degree of phenotypic diversity in poison ivy populations across North America (Barkley 1937, Gillis 1971). To what degree this phenotypic diversity is a manifestation of either innate phenotypic plasticity (i.e., the general-purpose genotype) or genetic adaptation of local populations is an important topic worthy of further research. Gillis (1971) identified suspected hybrid zones comprising populations with intermediate phenotypes. He also made presumed interspecific crosses that yielded individuals with intermediate morphological characters. Although these results indicate the presence of genetically differentiated populations, differences in morphological characters did not indicate whether the 2 parental Poison Ivy populations were differentially adapted for specific ecophysiological traits. Our study found Poison Ivy exhibited significant accession-level differential growth-responses, such as plant height, leaf Northeastern Naturalist 198 J.G. Jelesko, E.B. Benhase, and J.N. Barney 2017 Vol. 24, No. 2 area, chlorophyll level, total biomass, and root:shoot biomass. Moreover, there was significant accession-level variation in Poison Ivy plant height and leaf area in response to the light environment, and weak interaction between nutrient availability and chlorophyll content. These findings indicate that Poison Ivy phenotypic diversity extends beyond morphological characters, and includes presumed genetic adaptation of biometric ecophysiological traits that are likely important for the species’ success in specific disturbed or native habitats. Our conclusions might have been stronger if we had determined the taxonomic subspecies of each of the 4 lianas that gave rise to the 4 geographically isolated drupe accessions. Thus, future studies using a broader diversity of phytogeographical accessions (with T. radicans ssp. characterization) are needed to characterize the degree to which poison ivy exhibits local adaptation across diverse habitat types (Atwater et al. 2016). The observed poor growth of the Iowa accession was unexpected. We were unable to determine the environmental parameter that restricted the vigor of the Iowa accession in these experiments. Gillis (1971) reported that calcium deficiency has a profound effect limiting poison ivy growth and viability. In the present work, we used Hoagland’s solution, which contains calcium, as the base fertilizer; yet, neither full + N nor full - N fertilizer treatments improved overall growth of the Iowa accession relative to the control treatment (no Hoagland’s). Thus, the poor vigor of the Iowa plants was a consistent accession-level effect, likely caused by an underlying genetic deficiency that was not displayed in the other 3 Poison Ivy accessions. Clearly, Poison Ivy accessions vary in their growth form and response to environmental conditions. Lianas are known to have a variety of ecological impacts due to their structurally parasitic growth form and rapid response to disturbance (Horvitz and Koop 2001). Lianas have been shown to outcompete other plant species, reduce seedling recruitment, and reduce ecosystem carbon dynamics (Horvitz and Koop 2001). 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