Invasive Science and Management 2016 9:171–181

Photosynthetic Performance of Invasive Species ()

Kristine M. Averill, Antonio DiTommaso, Thomas H. Whitlow, and Lindsey R. Milbrath*

Knowledge of photosynthetic capacity is crucial for fully understanding a species’ invasive potential and for the development of appropriate control strategies. Although growth and reproductive data are available for the invasive swallowwort vines Vincetoxicum nigrum and V. rossicum, photosynthetic data are wanting. These herbaceous, perennial congeners were introduced from separate European ranges during the late 19th century and became invasive during the following century in the northeastern and southeastern Canada. Vincetoxicum nigrum has been observed growing mainly in high light environments, whereas V. rossicum occurs across a wide range of light environments, suggesting niche divergence and that different management strategies might be needed for the two species. In this work, we investigated whether the differing habitat associations of these species is reflected in their photosynthetic capacities and leaf morphology. Photosynthetic parameters and specific leaf mass were determined across a range of light environments represented by four field habitats (common garden, forest edge, old field, and forest understory) and two greenhouse environments (high and low light). In the high-light common garden habitat, V. nigrum achieved 37% higher maximum photosynthetic rates than V. rossicum, but photosynthetic performance of the two species was the same in the forest edge habitat. Additionally, species’ performance was virtually identical in high light, low light, and transitions between high and low light regimes in the greenhouse. Specific leaf mass of V. nigrum was 17% higher in the common garden and 19% higher in the greenhouse compared with V. rossicum. Both invasive Vincetoxicum spp. appear capable of growing within a broad range of light environments and their management should be similar regardless of light environment. Other explanations are required to explain the scarcity of V. nigrum in low light natural areas. Nomenclature: Black swallowwort, Vincetoxicum nigrum (L.) Moench. [ louiseae Kartesz & Gandhi]; pale swallowwort, Vincetoxicum rossicum (Kleopow) Barbar. [Cynanchum rossicum (Kleopow) Borhidi]. Key words: Apocynaceae, dog-strangling vine, exotic , forest understory, light environment, old field.

More biological data are needed to link plant-based if they also have high maximum photosynthesis rates (Amax) mechanisms to the competitive success and spread of (e.g., Baruch and Goldstein 1999; Durand and Goldstein introduced plant invaders (Mack et al. 2000). Introduced 2001; McDowell 2002; Pattison et al. 1998). Invasive species might successfully become invasive if they have plants have been associated with increased photosynthetic favorable traits such as a rapid growth rate, high capacity (Durand and Goldstein 2001; Penuelas et al. reproductive output, high seedling establishment, better- 2010). Importantly, competitive ability closely corresponds adapted genotypes, or a combination of traits (e.g., Bazzaz to photosynthetic performance (Pearcy et al. 1981), and in 1986; Rejma´nek 1996; Williamson and Fitter 1996). naturally occurring grassland communities, dominant Plants often achieve high rates of growth and reproduction species have higher photosynthetic rates than subdominant species (McAllister et al. 1998). Thus, determining DOI: 10.1614/IPSM-D-16-00015.1 photosynthetic capabilities of invasive introduced plants * First and second authors: Research Associate and Professor, is an important step toward a fundamental understanding Soil and Crop Sciences Section, School of Integrative Plant of their success in introduced ranges. In this study, we Science, Cornell University, Ithaca, NY 14853; third author: aimed to determine the photosynthetic parameters and leaf Associate Professor, Horticulture Section, School of Integrative morphology of two highly invasive congeneric plants, Plant Science, Cornell University, Ithaca, NY 14853; fourth author: Research Entomologist, USDA-ARS Robert W. Holley Vincetoxicum nigrum (L.) Moench. [Cynanchum louiseae Center for Agriculture and Health, Ithaca, NY 14853. Corre- Kartesz & Gandhi] (black swallowwort) and V. rossicum sponding author’s E-mail: [email protected] (Kleopow) Barbar. [Cynanchum rossicum (Kleopow) Bar-

Vincetoxicum spp. photosynthesis 171 specific light environments. These differences afford the Management Implications opportunity to study the photosynthetic traits of the invaders as related to their habitat specificity. Vincetoxicum nigrum and V. rossicum are problematic invasive During the last century, V. nigrum and V. rossicum have perennial vines in the northeastern United States and southeast- become increasingly problematic in natural areas and they ern Canada. Although several facets of their biology and ecology have been previously investigated, this is the first study of their concern land managers seeking to maintain diversity photosynthetic capacities. We found that V. nigrum has a higher (DiTommaso et al. 2005). The Vincetoxicum species are maximum photosynthetic rate than V. rossicum in a high-light herbaceous, perennial vines in the Apocynaceae (subfamily common garden, where both species were planted. In the Asclepiadoideae) and are native to distinct, non-overlap- introduced range, V. nigrum occurs almost exclusively in high- ping regions in Europe. In its native range of France, Italy, light habitats in natural areas and, although this species might perform better in high light environments, V. rossicum is an and the Iberian Peninsula, V. nigrum occurs in high light invader of both high- and low-light natural areas. Regardless, we and partially shaded habitats (R. Sforza, USDA-ARS found that the two species showed nearly identical patterns of European Biological Control Laboratory, personal com- photosynthetic response in an intermediate light forest edge munication). Vincetoxicum rossicum is native to Ukraine habitat, where they occurred naturally, and under high- and low- light greenhouse conditions. Generally, where light availability and southwestern Russia, where it also grows in high light was limited, the species performed the same, and only where light open meadow and partially shaded forest-steppe habitats was virtually unlimited (common garden) did V. nigrum show a (DiTommaso et al. 2005). The Vincetoxicum species were photosynthetic advantage over V. rossicum. Based on these results introduced into North America in the late 1800s, likely as and despite its general absence in low-light natural area habitats, ornamentals, and soon escaped cultivation (DiTommaso et V. nigrum appears photosynthetically capable of growing in lower al. 2005). The vines often form dense stands of 130 stems light habitats. Overall, this work suggests the invasive swallow- 2 wort species are similar to one another in photosynthetic m or more, with individual stems growing 1 to 2 m in capacities and should be managed with the same approach. length and producing 100 to 400 seeds stem1 (Averill et Knowing that both species have the physiological potential to al. 2011; DiTommaso et al. 2005; Sheeley 1992; Smith et invade high- and low-light habitats suggests that land managers al. 2006). Among New York State populations, Douglass cannot ignore either habitat in their planning. However, because the invaders are similar photosynthetically and in their rapid (2008) confirmed that V. nigrum and V. rossicum are growth and high seed production in high light environments, distinct species and that intraspecific genetic variation was management of high-light areas should be prioritized. Lastly, the minimal. Despite occurring in similar native range light species are expected to respond quickly to increases in light environments, the species appear to invade successfully availability (e.g., during forest canopy disturbance), suggesting that land managers need to be especially vigilant in such different light environments in the introduced range situations. (DiTommaso et al. 2005), suggesting that photosynthetic traits might differ between the two species. In this study, we report on the photosynthetic response barich] (pale swallowwort) that are continuing to expand to different light environments by the invasive V. nigrum their ranges in northeastern North America. and V. rossicum. Knowing how these invasive plants respond to various light environments will help land Congeneric species are expected to have similar managers more accurately target management tactics aimed physiological traits resulting from their shared evolutionary at controlling spread of the invaders. If the species have ´ history (Antunez et al. 2001), especially where their ranges similar photosynthetic responses, the same management overlap (Mack 1996). In contrast to this expectation and approach can be used for both species; however, dissimilar despite sharing introduced ranges in North America, the photosynthetic responses might cause managers to prior- invasive Vincetoxicum species appear to differ in their itize the management of one species over the other. Here habitat associations. Although the species are so similar that we explored intra- and interspecific physiological variabil- they can be confused with one another when not in flower ity, asking, respectively: (1) Does each species exhibit a (DiTommaso et al. 2005), numerous and recent field detectable gradient of response to variation in light observations at multiple sites indicate that V. nigrum rarely availability? (2) Do the species have different trends in occurs in shaded habitats and instead invades habitats with their responses to light? If interspecific differences exist, this higher light, whereas V. rossicum is a successful invader in would suggest a link between photosynthetic capacity and both high and low light habitats (Averill et al. 2011; the habitat association differences observed and would DiTommaso et al. 2005; Smith et al. 2006; authors’ indicate management divergence. We investigated Vince- observations). On invasion at a site (i.e., establishment and toxicum photosynthetic performance in two field sites, a continued population expansion), both species can form common garden site, and a greenhouse. This range of high density patches. This suggests that, in their introduced natural and controlled settings permits study of the species’ ranges, V. nigrum might only invade habitats with high photosynthetic response to multiple light environments. In light availability whereas V. rossicum is unconstrained by the greenhouse, we also tested the species’ photosynthetic

172 Invasive Plant Science and Management 9, July–September 2016 Table 1. Vincetoxicum species occurring in each study setting and corresponding light availability.

Study setting Species present Instantaneous light intensity General light availability

lmol m2 s1 Common garden V. nigrum and V. rossicum 1,762 6 13 High Forest edgea V. nigrum and V. rossicum 169 6 19 Intermediate Gully–old fielda V. rossicum 1,798 6 11 High Gully–foresta V. rossicum 21 6 4 Low Greenhouse V. nigrum and V. rossicum 909 6 318 High Greenhouse with shade cloth V. nigrum and V. rossicum 25 6 9 Low a Populations are naturally occurring. response to an increase or decrease in light availability to (Nursery Supplies Inc., Chambersburg, PA) filled with a determine how they respond to changes in available light. soilless growing medium (Metro-Mix 560, Sun Gro In high light environments (i.e., full-sun common garden) Horticulture Distribution Inc., Bellevue, WA), which were we expect that V. nigrum will have a higher maximum buried in trenches with the rims nearly flush with the soil, photosynthetic rate and specific leaf mass (SLM) than V. at a research site on the Cornell University campus rossicum. In intermediate- and low light environments (i.e., (428270N, 768270W) in Ithaca, Tompkins County, NY. forest edge and beneath shade cloth in the greenhouse), we The research site had no overarching canopy and spanned expect that V. rossicum will have a higher maximum approximately 25 by 20 m. Isolated plants (n ¼ 7) that were photosynthetic rate and SLM than V. nigrum. ~ 5 m away from one another were randomly chosen for photosynthesis measurements. Pots were weeded, and Materials and Methods surrounding vegetation was mowed regularly throughout the growing season. The plants had been growing in the We conducted this work in (1) naturally occurring and full-sun common garden location for more than a year common garden populations of Vincetoxicum species in before photosynthetic measurements were taken. This three locations in central New York state in late June and July 2008 and in (2) experimentally manipulated green- location provided a high light environment, with mean 6 SE instantaneous solar irradiance of 1,762 6 13 lmol house conditions in June 2012. Ambient light intensity was 2 1 measured on clear days using a 1-m LI-COR LI-191SA m s (measured July 23, 2015, in the same field). Plants ceptometer and a LI-COR LI-1400 data logger (LI-COR, were 40 to 65 m away from the wooded edge. Lincoln, NE) between 10:00 A.M. and 2:00 P.M., and Photosynthesis measurements were taken on two consec- except where noted, light measurements were taken directly utive days beginning on July 24, 2008. above plants used for measuring photosynthesis on the same days as when physiological data were collected. Forest Edge. Vincetoxicum nigrum and V. rossicum naturally co-occur along an urban forest edge habitat spanning ~ 80 Field Study. Each of the three field locations (common by 2 m, in Ithaca, Tompkins County, NY (428270N, garden, forest edge, and Gully) included either two species 768290W). Isolated plants (n ¼ 6) that were ~ 5 m away (V. nigrum and V. rossicum) or two habitat types (Table 1). from one another were randomly chosen for photosynthesis Plants used for physiological measurements were at the measurements. This location provided an intermediate same phenological growth stage—multistemmed and light environment, with instantaneous solar irradiance of reproductive. 169 6 19 lmol m2 s1 (mean 6 SE) along the edge, equating to 27% of sunlight in the adjacent opening, 620 2 1 Common Garden. In September 2006, V. nigrum plants 6 10 lmol m s . Photosynthesis measurements were were collected from Bear Mountain State Park, Rockland taken on two consecutive days beginning on June 30, 2008. County, NY (418180N, 738580W) and V. rossicum plants were collected from a private property near Elbridge, Gully. Vincetoxicum rossicum occurs naturally at the Great Onondaga County, NY (43800N, 768240W). Rootstocks Gully Nature Preserve in Union Springs, Cayuga County, were washed of soil and stored in moist vermiculite at 4 C NY (428480N, 768400W), where it grows across a light until they were transplanted the following spring in May gradient from an old-field habitat (~ 80 by 50 m) to a 2007. Rootstocks were planted in 23-L black plastic pots mixed deciduous forest understory habitat (~ 80 by 50 m).

Vincetoxicum spp. photosynthesis 173 Consequently, the Gully location provided two light treatment was achieved with 90% neutral density shade environments for study of V. rossicum, but not of V. cloth (Griffin Greenhouse, Auburn, NY) surrounding a nigrum. Isolated plants (n ¼ 6) that were ~ 10 m away 91 by 91 by 102-cm polyvinyl chloride frame. The low from one another were randomly chosen for photosynthesis light treatment (25 6 9 lmol m2 s1, n ¼ 5, noon on measurements. Instantaneous solar irradiance in the forest May 30, 2012, sunny conditions) was approximately understory (21 6 4 lmol m2 s1) was approximately 2.7% of light availability in the high light treatment (909 1.2% of light availability in the old field (1,798 6 11 lmol 6 318 lmol m2 s1). Initial photosynthesis measure- m2 s1). Forest understory sunflecks were short lived and ments were collected on June 16, 2012 (t ¼ Ø), after infrequent. In the old field, plants used in this study were which a subset of plants from each light environment was located within 20 m of the adjacent forest or small trees, transitioned to the opposite light environment. Photo- which were scattered through the field. Photosynthesis synthesis was measured again after transitions beginning measurements were taken on three consecutive days on June 27, 2012 (t ¼ 1). beginning on June 23, 2008. Photosynthesis Measurements. A LI-COR 6400 portable Greenhouse Study. In autumn 2010, mature rootstocks photosynthesis instrument with infrared gas analyzers (LI of V. nigrum and V. rossicum were collected from Bear COR, Lincoln, NE) was used to measure photosynthesis Mountain State Park and Robert G. Wehle State Park, with the following settings: LED red/blue light source, 0 0 1 Jefferson County, NY (43852 N, 76815 W), respectively. CO2 flow rate of 500 lmol s , and reference CO2 Rootstocks were washed of soil and stored in moist concentration of 400 lmol mol1.Theinstrument- vermiculite at 4 C until the following spring, when they automated calibration function was used before taking were transplanted individually into a soilless growing measurements each day. Net photosynthesis (CO2 assim- medium (Metro-Mix 560, Sun Gro Horticulture Distri- ilation on a per area basis) of the most recently expanded, bution Inc., Bellevue, WA) in 1.9-L plastic pots and mature, undamaged leaf that would fill the 2 3 3-cm fertilized using a 15–9–12 (N–P–K) plus micronutrient cuvette was measured. In the greenhouse study, measure- slow-release fertilizer (Osmocote Plus, Scotts-Sierra Hor- ments were collected from the same leaf before and after ticultural Products Co., Marysville, OH). Plants grew in a light environment transition. Photosynthesis was measured shade house during 2011 and, after senescing that across a range of irradiances from 0 to 2,000 lmol m2 s1 autumn, were again stored at 4 C until photosynthesis photosynthetic photon flux density (PPF; ¼ photosynthet- experiments began the following spring. Beginning on ically active radiation). In the field, 11 levels of irradiance May 21, 2012, individual plants were randomly assigned were used, and in the greenhouse 9 levels were used. We to high or low light treatments in a greenhouse began the measurements at 500 PPF and increased to maintained at 25/20 C with supplemental 400 W high- 2,000 in a stepwise manner before returning to 500 PPF pressure sodium lights set for a 14/10 h day/night cycle. and decreasing stepwise to 0 PPF to measure dark The alternating photophase was the same for high and low respiration. At each level of irradiance, we waited for light conditions. We used a split-plot randomized plants to reach a steady rate of photosynthesis before complete block design with species (V. nigrum or V. recording the measurement. During each day of the field rossicum)asthesubplottreatmentandlightenvironment study, paired sets of photosynthesis measurements were as the main plot treatment. Four light environment collected from each species (at common garden and forest treatments were tested: (1) high light at time t ¼ Øand edge locations) or habitat (field and forest at Gully high light at time t ¼ 1, (2) high light at time t ¼ Øand location). In the field study, the LI-COR 6400 chamber low light at time t ¼ 1, (3) low light at time t ¼ Øand temperature varied within 1.5 C of the 27 C mean, except high light at time t ¼ 1, and (4) low light at time t ¼ Ø on three days when early morning temperatures were as low andlowlightattimet ¼ 1. Five blocks were used with one as 21 C and afternoon temperatures as high as 28 C. For individual plant of each species in each light environment this reason, temperature was included as a covariate in treatment per block. The photoperiod naturally changed modeling procedures for the field study. Chamber air over the course of the experiment (May to June), temperature was held constant at 20 C in the greenhouse increasing to a maximum photophase of 15 h 18 min study. Plants grown under low light conditions in the (sunrise to sunset). Plants were watered daily. The high greenhouse were allowed to acclimate under ambient light condition consisted of growing plants on bench tops greenhouse light conditions before measurements were subjected to ambient greenhouse light, and the low light taken.

174 Invasive Plant Science and Management 9, July–September 2016 Specific Leaf Mass. Plant tissue samples were collected error rates. For field data, we used ANOVA to determine from individual Vincetoxicum leaves on separate plants, the effects of species or light environment on SLM, with a carefully avoiding the midvein, from each species in each separate ANOVA for each field location. For greenhouse light environment. Disc-shaped samples from field (n ¼ 10 data, we used mixed effects ANOVA to determine the or 11) and greenhouse (n ¼ 5) plants were 18 and 10 mm effects of species, light environment, and their interaction on SLM with block as the random effect. We used the least diam, respectively. Samples in the field study were taken significant difference test for pairwise comparisons (a ¼ from different plants than those used for photosynthesis 0.05). We used linear regression to test for a correlation measurements, whereas samples in the greenhouse study between mean SLM and Amax across field habitats. We used were taken from the same plants as photosynthesis R version 2.9.2 (R Development Core Team 2006) for measurements. Discs were dried for 48 h at 65 C before statistical analysis and the gnls function, which fits a weighing. To determine SLM (g m2), we divided the mass nonlinear model using generalized least squares, in the of the dry disc by the initial disc area. nlme package for nonlinear modeling (Pinheiro et al. 2016). Statistical Analyses. Three photosynthetic curve parame- ters were estimated using the Mitscherlich model, as Results and Discussion described in Potvin et al. (1990) and Peek et al. (2002) (Equation 1): To answer our first study question, the two invasive hiVincetoxicum species varied intraspecifically according to A ¼ A 1 eAqeðPPFLCPÞ ð1Þ the light environments investigated, suggesting that they max each exhibit a gradient of response to variation in light availability. To answer our second study question, where A is net photosynthesis (dependent variable), Amax is the asymptote of the curve at high light (light-saturated or interspecifically, the species did not have different trends in their responses to light and performed similarly to one maximum rate of photosynthesis), Aqe is the initial slope of another in photosynthetic parameters within most light the curve at low light levels (quantum yield), and LCP environments. These results imply that photosynthetic (light compensation point) is the x-intercept. PPF, the only response and the habitat association differences observed independent variable, refers to the incident light on the leaf between the species are unrelated or weakly related. emitted by the LI-COR 6400 instrument. The LCP is the point at which net photosynthesis is zero (photosynthetic Field Study. Among field habitats, photosynthetic perfor- gain ¼ respiration), and Aqe (¼ quantum yield) is a measure mance of both species was greatest in the high-light of photosynthetic efficiency. Shade-adapted individuals are common garden habitat (Figures 1A–C and 2). Vincetox- expected to have lower photosynthesis rates and light icum nigrum achieved a model-fitted, maximum photo- compensation points and higher quantum yields than sun- synthetic rate (Amax) that was 37% higher than for V. adapted individuals (Taiz and Zeiger 2002). Separate rossicum (23 6 2 lmol m2 s1 vs. 17.0 6 0.9 lmol m2 models for net photosynthesis were developed for each s1) (Figure 2A) in the common garden. In this habitat, species in each light environment, allowing for a reduction photosynthetic efficiency (Aqe) or quantum yield of V. in parameterization and an increased level of confidence for rossicum was 39% higher than for V. nigrum (0.0033 6 the three photosynthetic parameters of interest. 0.0001 vs. 0.0023 6 0.0003) (Figure 2B), and the light Plant identification was included as a random effect in compensation point (LCP; net photosynthesis is equal to the photosynthetic curve models to account for repeated zero) did not differ between species (Figure 2C). The SLM measurements on the same leaf (Peek et al. 2002). A fixed of V. nigrum was 17% greater than for V. rossicum (84 6 2 variance structure was specified in each model, which gm2 vs. 72 6 1gm2) in the common garden habitat allowed for the larger residual spread as PPF increased (F ¼ 27, P , 0.001) (Figure 3A). These results suggest without requiring additional parameters (Zuur et al. 2009). 1,45 We used the confidence interval overlap method to that only in this high light environment do Vincetoxicum compare the fitted photosynthetic curve parameters derived species have different trends in their responses to light and from each of the models for the field study and separately support our expectation that V. nigrum would have a for the greenhouse study. We used 84% confidence higher Amax rate and SLM than V. rossicum in the intervals to best approximate the a ¼ 0.05 hypothesis test environment with the highest light availability. Plants with (Payton et al. 2003). Using 95% confidence intervals high photosynthesis rates are well adapted to high light would have provided overly conservative results and using environments. Additionally, leaves with high photosynthe- standard error intervals would have yielded higher type I sis rates often exhibit high SLM (i.e., thicker leaves, greater

Vincetoxicum spp. photosynthesis 175 Figure 1. Model-derived photosynthetic curves for the invasive vines Vincetoxicum nigrum and V. rossicum in three central New York state field habitats—(A) a high-light common garden (n ¼ 7), (B) an intermediate-light urban forest edge (n ¼ 6), and (C) for V. rossicum only, adjacent forest and old-field habitats (n ¼ 6)—and under greenhouse conditions with (D) high light, (E) low light, and (F, G) transitions between high and low light. Greenhouse data were collected at two time points (t ¼ Ø and t ¼ 1), separated by 8–11 d(n ¼ 5). Error bars are excluded for clarity. Refer to Figures 2 and 4 for statistical interpretation.

176 Invasive Plant Science and Management 9, July–September 2016 Figure 3. (A) Specific leaf mass (means 6 SE) for Vincetoxicum nigrum and V. rossicum in four central New York state habitats varying in light availability (n ¼ 10–11). (B) Change in specific leaf mass (means 6 SE) from time t ¼ Øtot ¼ 1, separated by 8–11 d, in high- and low-light greenhouse conditions (n ¼ 5). Asterisks above/below bars indicate the change is significantly different from zero (a ¼ 0.05). leaf density, or both), because sun leaves are thicker than shade leaves in deciduous species (e.g., Hanson 1917; Oguchi et al. 2003). Vincetoxicum nigrum appears well adapted for high light environments, and this finding is consistent with the apparent restriction of this species mainly to habitats with high light availability in its introduced range (DiTommaso et al. 2005; authors’ observation). Correspondingly, V. nigrum vegetative ex- pansion rates in old fields can be greater than those of V. rossicum (Averill et al. 2011), and V. nigrum plants produce more overall biomass and seed under greenhouse condi- tions than V. rossicum (Milbrath 2008). Vincetoxicum nigrum has a lower root-to-shoot ratio and thus allocates

Figure 2. Model-derived photosynthetic parameters (means 6 SE) for Vincetoxicum nigrum and V. rossicum in high-light common garden and intermediate-light forest edge habitats and, for V. rossicum only, in forest and old-field habitats in central New York state (n ¼ 6–7). (A) Maximum photosynthesis. (B) Quantum yield. (C) Light compensation point. Bars with different letters indicate significant differences between species and among habitats (a ¼ 0.05).

Vincetoxicum spp. photosynthesis 177 more biomass to shoots than to roots than V. rossicum photosynthesis and leaf surface area–to–mass ratio has (McKague and Cappuccino 2005; Milbrath 2008). been observed across hundreds of species distributed However, V. rossicum often produces more seeds per stem globally (Reich et al. 1997). under high light field conditions compared with V. nigrum Vincetoxicum rossicum photosynthetic rates were (Averill et al. 2011), and despite having smaller seeds, V. lowest in the forest habitat among the field habitats investigated, as would be expected of shade-dwelling rossicum typically produces more seedlings per seed than V. individuals. Additionally, Amax rates were similar to or nigrum (both species are polyembryonic) (DiTommaso et higher than those previously reported for noninvasive, al. 2005). Under the optimal growing conditions in the native, perennial forest floor plants. The Amax rate of V. common garden, the Vincetoxicum species had similar or rossicum (7.1 6 0.4 lmol m2 s1) exceeded those higher Amax rates (Figure 2) than those reported elsewhere reported for the following co-occurring native forest for early- (~ 16 lmol m2 s1) and mid- (10 lmol understory species at the end of June or in early July: m2 s1) successional species (Bazzaz and Carlson 1982; white trillium [Trillium grandiflorum (Michx.) Salisb.] Zhang et al. 2009). (4 lmol m 2 s 1), mayapple (Podophyllum peltatum L.) 2 1 In contrast to physiological differences observed between (4 lmol m s ), zigzag goldenrod (Solidago flexicaulis 2 1 the Vincetoxicum species under high light conditions, the L.) (4 lmol m s ), and Virginia-creeper [Partheno- 2 1 two species performed the same along the forest edge, an cissus quinquefolia (L.) Planch.] (4 lmol m s )(Taylor intermediate light–availability habitat. Along this urban and Pearcy 1976). We calculated relatively low LCP roadside edge, no differences between species were observed values for V. rossicum in the forest understory, which in model-fitted estimates of Amax, Aqe, or LCP (Figure 2) or allows the species to maintain a positive carbon balance in SLM (F1,56 ¼ 1.1, P ¼ 0.29) (Figure 3A). The fact that under shade. The LCP we observed for V. rossicum in the both invaders naturally occur at this location supports the forest habitat was lower than that reported for other forest understory species. For example, the LCP of finding that they are physiologically similar. The result 2 1 along the forest edge habitat was contrary to our mayapple is near 9 lmol m s PPF (Sparling 1967), whereas V. rossicum can compensate for respiration at expectation of a divergence in photosynthetic response 2 1 between the species. about 2 lmol m s PPF. Efficient photosynthetic physiology might help explain why V. rossicum can The Amax rate of V. rossicum was 40% higher in the common garden habitat than in the Gully old-field persist in low light environments. In forest understories, habitat, likely because of the lack of competition in the V. rossicum vegetative expansion rates are slow, and weeded common garden pots and because of shading plants produce little or no seed until light availability from scattered trees in the old-field habitat. In the old- increases after disturbance (Averill et al. 2011). Vince- field habitat, the maximum photosynthetic rate of V. toxicum species store resources in perennial belowground rossicum was similar to native, co-occurring midsucces- rootstocks (DiTommaso et al. 2005), which allows for a sional species, such as hairy white oldfield aster rapid growth response to increased light. In the face of [Symphyotrichum pilosum (Willd.) G.L. Nesom var. natural or anthropogenic disturbances that reduce pilosum (¼ Aster pilosus Willd.)] (13 lmol m2 s1) overstory cover where V. rossicum is ‘‘sitting and (Bazzaz 1979) and Canada goldenrod (Solidago cana- waiting’’ (sensu Greenberg et al. 2001), this species is densis L.) (~ 14 lmol m2 s1) (Wang et al. 2008). The likely to expand its dominance. Amax estimate for V. rossicum was 66% greater in Gully, the old-field habitat, compared with the adjacent forest Greenhouse Study. Within the greenhouse setting, the habitat (11.8 6 0.8 lmol m2 s1 vs. 7.1 6 0.4 lmol two Vincetoxicum spp. performed similarly, which again 2 1 m s ). The Aqe estimate observed in the old-field was contrary to our expectation of differences between habitat was 55% lower than that observed in the forest them (Figures 1D–G and 4). No significant differences habitat (0.0046 6 0.0005 vs. 0.0102 6 0.0007) (Figure between the species were found in model-fitted Amax and 2B). The LCP estimate was approximately five times A estimates for any of the treatments (Figures 4A and greater for V. rossicum in the common garden habitat (22 qe 4B). Overall, plants initially grown under high light 6 2 lmol m2 s1) and in the Gully old-field habitat (21 2 1 sustained high rates of photosynthesis even after more 6 2 lmol m s ) than in the Gully forest habitat (3.7 6 0.4 lmol m2 s1) (Figure 2C). Old-field plants had than a week exposed to lower light. The converse was also 230% greater SLM than forest plants (50 6 2gm2 vs. true; plants initially exposed to low light continued to 2 15.1 6 0.3 g m )(F1,40 ¼ 337, P , 0.001) (Figure 3A). photosynthesize at reduced rates after their transition to Across species and habitats, Amax values were positively the higher light environment. For these Vincetoxicum correlated with SLM (slope ¼ 0.23, R2 ¼ 0.91, P ¼ species, the time period (8 to 11 d) between t ¼ Øandt ¼ 0.003). Consistently, a positive relationship between 1 appears too short for net photosynthesis or Aqe to

178 Invasive Plant Science and Management 9, July–September 2016 ments in the greenhouse. LCP estimates declined for plants that transitioned from high to low light, and LCP estimates increased for plants that transitioned from low to high light. After the transition from high to low light treatment, the LCP of V. rossicum was lower than for V. nigrum, which suggests that V. rossicum might be better at quickly adapting to a lower light environment than V. nigrum.In the low-light control group, the LCP of V. nigrum was higher than for V. rossicum at t ¼ Ø, and the reverse was found at t ¼ 1 (Figure 4C). For V. nigrum in the low-light control group, the Aqe estimate declined from t ¼ Øtot ¼ 1; the LCP estimate for V. nigrum under this treatment also declined over the 8- to 11-d period. Also in the low-light control group, the LCP of V. rossicum increased from t ¼ Ø to t ¼ 1. A possible reason why plants in the low-light control group did not have the same Aqe or LCP estimates during the experiment include starch accumulating in the measured leaves, which can produce an inhibitive effect on net CO2 assimilation (Azcon-Bieto´ 1983). In the greenhouse, SLM was highest under high light and lowest under low light (Figure 3B). SLM varied by species (F1,64 ¼ 42, P , 0.001) and by light environment (F7,64 ¼ 144, P , 0.001), but not by their interaction (F7,64 ¼ 1.5, P ¼ 0.18). Vincetoxicum nigrum (181 6 12 g m2) had 19% higher SLM than V. rossicum (152 6 10 g m2). SLM increased by 150% in the transition from low to high light and the transition from high to low light resulted in a significant decrease of 20% (Figure 3B). SLM increased in the control groups from t ¼ Øtot ¼ 1by25to 34%, which likely accounts for some of the increase observed in the transition from low to high light. Interestingly, SLM in the greenhouse was more than twice that observed in field locations (Figure 3). Overall, both species have the physiological potential to Figure 4. Change in model-derived photosynthetic parameters invade habitats with high and low light availability, between time t ¼ Øtot ¼ 1 separated by 8–11 d for Vincetoxicum indicating that land managers ought not to ignore either nigrum and V. rossicum under greenhouse conditions with high type of habitat. Because Vincetoxicum spp. achieve faster light, low light, and transitions between high and low light (n ¼ growth and higher seed production in high light 5). (A) Maximum photosynthesis. (B) Quantum yield. (C) Light compensation point. Asterisks above/below bars indicate the environments (Averill et al. 2011), management of these change is significantly different from zero (a ¼ 0.05). areas needs to be prioritized. Where either invader occurs in forests that are expected to be disturbed, managers should be especially vigilant because the species perform respond to changes in light environment. In contrast, best in high light environments. photosynthesis in common lambsquarters (Chenopodium album L.) has been shown to respond to altered light Acknowledgments availability within 4 d (Oguchi et al. 2003). A longer term transition experiment in which Amax rates responded to The authors thank Scott Morris, Andrew Ebanks, Melanie altered light availability would be necessary to test for Ho, and Johnny Means for valuable field and laboratory evidence of phenotypic plasticity in the invasive Vincetox- assistance. Matt Ryan, Tyler Wagner, Emily Rauschert, icum spp. and to test for effects of forest canopy removal Stephane´ Cordeau, and members of the Landscape Ecology or addition. at Penn State group provided valuable feedback on earlier Vincetoxicum LCP estimates responded largely as would manuscript drafts. The authors thank The Nature Conser- be expected during the transitions between light environ- vancy for permission to conduct research in the Great Gully

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180 Invasive Plant Science and Management 9, July–September 2016 Wang D, Heckathorn SA, Mainali K, Hamilton EW (2008) Effects of Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed N on plant response to heat-wave: a field study with prairie Effects Models and Extensions in Ecology with R. New York: vegetation. J Integr Plant Biol 50:1416–1425 Springer. 580 p Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666 Zhang Z, Jiang C, Zhang J, Zhang H, Shi L (2009) Ecophysiological Received February 23, 2016, and approved July 11, 2016. evaluation of the potential invasiveness of Rhus typhina in its non- native habitats. Tree Physiol 29:1307–1316 Associate Editor for this paper: John Cardina, Ohio State University.

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