Plant Ecol (2010) 211:65–77 DOI 10.1007/s11258-010-9773-2

Establishment of the invasive perennial rossicum across a disturbance gradient in New York State, USA

Kristine M. Averill • Antonio DiTommaso • Charles L. Mohler • Lindsey R. Milbrath

Received: 23 October 2009 / Accepted: 7 April 2010 / Published online: 22 April 2010 Ó Springer Science+Business Media B.V. 2010

Abstract Vincetoxicum rossicum (pale swallow- tillage and herbicide-only plots [1.6 ± 0.5%]. Of those wort) is a non-native, perennial, herbaceous vine in seedlings that emerged, overall survival was high at the . The species’ abundance is steadily both locations (70–84%). Similarly, total (above ? increasing in the northeastern United States and belowground) biomass was greater in herbicide ? till- southeastern Canada. Little is known about Vincetox- age and herbicide-only plots than in mowed and icum species recruitment and growth. Therefore, we control plots at both locations. Thus, V. rossicum was conducted a field experiment in New York State to successful in establishing and surviving across a range address this knowledge gap. We determined the of disturbance regimens particularly relative to other establishment, survival, and growth of V. rossicum old field species, but growth was greater in more during the first 2 years after sowing in two old fields disturbed treatments. The relatively high-establish- subjected to four disturbance regimens. We hypothe- ment rates in old field habitats help explain the sized that establishment and survival would be higher invasiveness of this Vincetoxicum species in the in treatments with greater disturbance. At the better- northeastern U.S. and southeastern Canada. drained location, overall establishment was 15 ± 1% [mean ± standard error] and did not differ among Keywords Biotic resistance Dog-strangling vine treatments. At the poorly drained location, establish- Environmental gradient Invasibility ment varied by treatment; mowed and control plots had Pale swallow-wort Weed ecology greater establishment [10 ± 2%] than herbicide ?

Introduction

K. M. Averill A. DiTommaso (&) C. L. Mohler Department of Crop and Soil Sciences, Cornell A species must overcome a cascade of limiting factors University, Ithaca, NY 14853, USA to become invasive (Gordon 1998; Williamson 2006). e-mail: [email protected] Enough propagules must be transported from the native range for a population to establish. Recruitment Present Address: K. M. Averill is a critical phase in the invasion process, during which Department of Crop and Soil Sciences, The Pennsylvania high rates of mortality may occur (Jesson et al. 2000; State University, University Park, PA 16802, USA Lockwood et al. 2005); it is driven largely by biogeographical and ecological factors (Williamson L. R. Milbrath USDA-ARS Robert W. Holley Center for Agriculture 2006). Gurvich et al. (2005) suggest that once an and Health, Ithaca, NY 14853, USA invader becomes established, the invaded habitat must 123 66 Ecol (2010) 211:65–77 satisfy only one or a few characteristics to ‘‘trigger’’the held constant the propagule pressure (number of spread and invasion of the species. Abiotic constraints individuals per unit area) (Lockwood et al. 2005) and play a dominant role in invasibility of habitats and, in time since introduction (by using one sowing date). suitable environments, invasives must additionally We also controlled for autecology by only examining overcome biotic constraints (Gerhardt and Collinge one species and genetic variation because propagules 2007). Early successional habitats, such as old fields, were collected from one population. Using only one are particularly prone to invasion due to their vulner- population was valid because genetic similarity is able state of transition (Johnson et al. 2006). high among introduced V. rossicum populations in One area of focus in the plant invasion literature is New York (Douglass 2008; Douglass et al. 2009). We the attempt to find commonalities among habitats that varied the intensity of old field disturbance. We used increase their susceptibility to invasion. Disturbance mowing, herbicide applications, and tillage to deter- allows a direct or indirect increase in available mine the response of V. rossicum to different distur- resources (Sousa 1984), including light, nutrients, and bance regimes. This approach tested the fluctuating water previously utilized by the resident vegetation resource hypothesis of invasibility (Davis et al. 2000), (Canham and Marks 1985). Even brief disturbances which proposes that plant species may successfully allow a pulse of resources to be released that can establish in novel habitats when their propagules temporarily reduce competition and increase suscep- encounter unexploited resources such as light, mois- tibility to invasion (Davis et al. 2000; Davis and ture, or nutrients. We predicted that V. rossicum Pelsor 2001; Yang et al. 2008). Many non-indigenous establishment success and growth would be the lowest species can establish by taking advantage of such in the control treatment, where competition would be disturbed habitats (Gray et al. 1987; Hobbs 1989; strongest (intact old field community), and that Hobbs and Huenneke 1992; Orians 1986). Vincetox- establishment and growth would increase with icum rossicum (Kleopow) Barbar. = increasing disturbance intensity. rossicum (Kleopow) Borhidi (pale swallow-wort) is one invader that we hypothesized would have a high potential for exploiting resources after disturbances. Materials and methods Thus, V. rossicum was the focus of the experiments reported here. Study species In order to improve management of invasive , the use of manipulative field experiments that aid in Vincetoxicum rossicum (Apocynaceae, subfamily determining which habitats or plant communities can Asclepiadoideae) is native to the Ukraine and South- resist or are susceptible to invasion has been proposed western Russia where it grows on stony meadow (Bergelson et al. 1993; Davis et al. 2000; Levine and steppe habitats and on rock outcrops (DiTommaso D’Antonio 1999). However, the multiple interacting et al. 2005b). The species was introduced into North factors that contribute to invasion success need to be America in the late-1800s (Moore 1959), probably as considered in such studies (Hobbs and Humphries an escaped ornamental (Sheeley and Raynal 1996). Its 1995). In the experiment reported here, we adhered to current distribution extends from the Atlantic coast the research framework proposed by Barney and west to southern Michigan and northern Indiana, and Whitlow (2008) in their state factor model for from southern Ontario, Canada, south to southern biological invasions. They presented five state factors, Pennsylvania (DiTommaso et al. 2005b; Sheeley and including propagule pressure, introduced habitat, Raynal 1996). V. rossicum is a twining herbaceous invader autecology, source environment and genetic perennial vine that can grow up to 3 m long in one variance, and time since introduction, and suggested growing season (Averill et al. unpublished) and that more experimental evidence with consideration exhibits relatively high fecundity (Averill et al. for these state factors is required to elucidate invasion unpublished; Sheeley 1992; Smith et al. 2006). The success and provide managers with a more holistic species reproduces and invades new sites by seed, but view of the invasion (Barney and Whitlow 2008). In plants can also grow and expand via buds on root our 2-year study, we controlled for four of the five crowns (Averill et al. unpublished; DiTommaso et al. state factors, while manipulating a fifth factor. We 2005b). V. rossicum seeds, like other members in the 123 Plant Ecol (2010) 211:65–77 67

Apocynaceae, have silky, parachute-like appendages elevation 317 m). V. rossicum is uncommon at both (coma) that assist in wind dispersal. Seeds are often locations; only one mature plant was found 20 m polyembryonic, giving rise to as many as six multiple from the hill top experiment. Despite the ability of seedlings independently of seed mass (Cappuccino V. rossicum to thrive in low light environments, et al. 2002; DiTommaso et al. 2005b). This invasive management in high light habitats is of foremost vine has shown variable emergence and survival in concern, since reproductive output and plant expan- field and glasshouse conditions (Cappuccino et al. sion is greater in such environments (Averill et al. 2002; DiTommaso et al. 2005a; Ladd and Cappuccino unpublished; Hotchkiss et al. 2008; Smith et al. 2005). Emergence (50–72%) and survival (71–100%) 2006). Prior to the start of our study, the hill top and were high in a relatively undisturbed 5-year old field plateau locations had not been mowed for 1 and in Ontario, Canada (Ladd and Cappuccino 2005). 5 years, respectively. Mature V. rossicum plants exhibited 99–100% sur- In November 2007, we collected soil samples from vival during a 4-year field study (Averill et al. each location to determine pH, soil organic matter unpublished), demonstrating that, once established, (SOM) derived from loss on ignition (Storer 1984), these plants have high survival rates. and percentage moisture. The hill top location is on a Vincetoxicum rossicum is increasingly problematic Mardin channery silt loam (course-loamy, mixed, in a range of habitats including old fields, pastures, active, mesic typic fragiudepts), which is a moder- no-tillage agricultural fields, Christmas tree planta- ately well-drained soil with pH 5.3 and 4.6% soil tions, forest understories, and roadsides (DiTommaso organic matter (SOM). The plateau location is on an et al. 2005b). In the globally rare alvar communities Erie channery silt loam (fine-loamy, mixed, active, (sub-boreal limestone barrens) near Lake Ontario, mesic aeric fragiaquepts), which is a somewhat large areas have been infested with this invasive vine poorly drained soil with pH 6.1 and 4.8% SOM. (DiTommaso et al. 2005b). The species tolerates a Both locations were uniformly free of large stones wide range of moisture conditions and light environ- and parent material. The plateau location soil had ments. The roots of V. rossicum likely contain the 70 ± 10% moisture content, so at the time of hemolytic glycoside vincetoxin, which is considered sampling was wetter than the hill top location, which poisonous to mammals, including humans (Alex and had 50 ± 10% moisture content. Switzer 1992). Monarch butterflies sometimes ovi- Based on visual assessments, the hill top location posit on V. rossicum (Casagrande and Dacey 2007), was dominated by Poa pratensis L. (Kentucky blue- resulting in no larval survival or growth compared grass) (46%), Galium mollugo L. (smooth bedstraw) with larvae from eggs oviposited on the native (37%), Dactylis glomerata L. (orchard grass) (22%), Asclepias syriaca L. (common milkweed) (DiTomm- and Schedonorus phoenix (Scop.) Holub (tall fescue) aso and Losey 2003; Mattila and Otis 2003). Anec- (21%) [ according to USDA-NRCS (2010)]. dotal evidence suggests that dense populations of The plateau location was dominated by Solidago V. rossicum deter grassland birds from nesting in the altissima L. (tall goldenrod) (41% cover), P. pratensis summer and prevent raptor predation of small rodents (25%), Phalaris arundinacea L. (reed canarygrass) who may take refuge under the tangle of dead vines (16%), and G. mollugo (15%). in the winter (DiTommaso et al. 2005b). Furthermore, research has shown that V. rossicum can modify Disturbance treatments arbuscular mycorrhizal fungal communities, possibly altering succession (Greipsson and DiTommaso 2006; We quantified V. rossicum emergence, survival, stem Smith et al. 2008). length, root-to-shoot ratio, and phenology in a range of disturbance regimens during 2 years. The four Study locations disturbance treatments, in order of increasing inten- sity, were (1) undisturbed old field (control), (2) We conducted this experiment in two herb-dominated mowing resident vegetation to a height of 20 cm old fields near Ithaca, NY. One location was on a hill annually, (3) killing vegetation using herbicides, and top (42°270 N, 76°220 W, elevation 518 m) and the (4) killing vegetation using herbicides plus tillage. other was on a lower plateau (42°290 N, 76°260 W, These disturbance treatments were chosen to reflect 123 68 Plant Ecol (2010) 211:65–77 habitats currently colonized by V. rossicum, including Planting abandoned agricultural land at different stages of succession, mowed roadsides, and hayfields mowed We collected *5,000 seeds from 50 randomly once per year. Thus, whereas the herbicide and selected plants in a population *45 km northwest of herbicide plus tillage treatments may provide brief the experimental locations at The Nature Conservancy but relatively high resource pulses, the mowing Great Gully Nature Preserve, Springport, NY (42°480 treatment provides repeated but lower resource pulses N, 76°410 W). Only filled (viable) seeds were used for (Yang et al. 2008). this experiment (Cappuccino et al. 2002); we found We established the experiment at each location in that 52 ± 2% of seeds per follicle were filled. We an eight-replicate randomized complete block design determined percentage germination of five replica- with plots measuring 1.8 by 15.8 m. Plots were tions of 20 filled seeds each under controlled environ- separated by 3 m mowed alleys. We included each ment conditions. After a 4-month moist stratification disturbance regimen in each block in a spatially period, 87 ± 4% of seeds germinated. Of germinated balanced design to reduce the effects of spatial seeds, 34% produced a single seedling, 52% produced variability of soil and vegetation (van Es and van Es two seedlings, 11% produced three seedlings, and 2% 1993). On 24 August 2006, we mowed the vegetation produced four seedlings. in plots that were to receive treatments 2, 3, and 4 to a On November 15, 2006, we planted V. rossicum height of 20 cm, leaving plant residues in place. On seeds in a grid design with two rows per plot. September 22, 2006, we applied the herbicides: Planting locations (sub-locations) were 0.5 m apart glyphosate [isopropylamine salt] (3.7 kg ai ha-1), a between and within rows. At each planting location, broad spectrum herbicide, and dicamba [diglycol- we planted two seeds 4 cm apart just below the soil amine salt] (3.0 kg ai ha-1), a broadleaf specific surface (2 mm) for a total of 60 seeds sown per plot. herbicide, to plots in treatments 3 and 4. We applied a second application of glyphosate to treatment 3 plots Data collection on May 11, 2007 prior to the emergence of V. rossicum seedlings. We did not re-apply dicamba in May 2007 We recorded the presence, length to apical meristem, to treatment 3 plots because of the residual activity of and number of stems of V. rossicum plants at each this herbicide, which could have affected V. rossicum sub-location every 3 weeks from May to October emergence. We applied the herbicides using a low- 2007 and May to August 2008. Ò volume, CO2-pressurized, Field King backpack We harvested above- and belowground biomass of sprayer [The Fountain Group, Inc., D. B. Smith & V. rossicum on August 25–29, 2008 and included root Co., Inc. (Affiliate), Utica, NY, USA]. Three weeks crowns as belowground biomass. We harvested shoot after the application of herbicides (October 13, 2006), biomass and recorded the number of nodes per stem. we tilled the soil in treatment 4 plots to a depth of about We harvested belowground plant tissues from three 15 cm using four passes of a tractor-mounted rotary randomly selected plants per plot, if present, and then tiller. Treatment 4 had three disturbances, each washed roots, dried above- and belowground portions delivered about a month apart. In the mowed-only for 48 h at 65°C, and weighed the tissue to determine treatment 2 plots, we mowed again on July 29, 2007 dry mass. We determined the mean plant biomass, and July 23, 2008. root and shoot biomass, root-to-shoot ratio, and The herbicides only partially killed the vegetation. number of nodes per stem for each plot at each Some species in the Asteraceae (e.g., S. altissima) location, and then removed all remaining root crowns were not controlled with the fall 2006 application of to preclude long-term V. rossicum establishment at the selective herbicide dicamba and were not affected the locations. We returned to the locations on July 16, by the spring 2007 glyphosate application since the 2009 to record any additional seedling emergence application was carried out very early in the growing and to remove newly emerged plants. We determined season. However, application of glyphosate was the mean plant biomass, root and shoot biomass, root- effective in limiting the cover of perennial grasses to-shoot ratio, and number of nodes per stem for each (e.g., P. pratensis and P. arundinacea). plot at each location.

123 Plant Ecol (2010) 211:65–77 69

In order to describe the presence of resident covariance (ANCOVA) to test for the effect of vegetation, we grouped old field species into 10 root-to-shoot ratio on our fixed effects by including categories: Aster plus Solidago spp., G. mollugo, root biomass and the interaction of root biomass with Rubus spp., other perennial broadleaf plants, annual treatment as covariates in a model with shoot biomass broadleaf plants, perennial grasses, annual grasses, as the response variable. For effects that were woody shrubs, sedges, and V. rossicum. To objec- significant at P \ 0.05, we used the least significant tively assess the abundance for each category, we used difference test for pairwise comparisons. a point intercept method to determine percentage We also tested the effects of location, treatment, cover. The point quadrat consisted of a 1.2 9 1.2 m and their interaction on survivorship curves using aluminum frame with two horizontal planes of cross Cox’s (1972) proportional hazards model, which wires separated vertically by 20 cm. Within each assumes that the hazard function is constant over time plane, cross wires formed 10 9 10 cm squares. and uses chi-square analysis for effect tests (see Adjustable wooden legs at the corners allowed Allison 1995). Of 637 emerged seedlings, 441 were quadrat leveling in the field. Looking down with one censored because they were still alive at the end of eye across a pair of cross wires provided a dimen- the experiment (August 2008). In our model, we used sionless line straight to the ground. At each line, we censorship as a way to account for the lack of recorded a ‘‘hit’’ for each unique vegetation category V. rossicum death dates in almost 70% of individuals laying directly below that pair of cross wires. Thus, (for details, see Allison 1995). each line may have hit several categories. We In order to test for the effect of abundance of recorded a hit for the ground if no vegetation was competing vegetation (using point intercept data) on present. On August 6–10, 2007 and July 14–17, 2008, V. rossicum emergence, survival, and total biomass, we collected data at 30 lines in each of four randomly we used ANCOVA with 2007 and 2008 vegetation placed quadrats in each plot (120 lines per plot). (total percentage cover) as covariates along with Additionally, in 2008, we recorded all species location, treatment, and their interaction. To test for present in each plot and the same observer made a the effect of relative cover of competing vegetation, visual estimate of percentage cover. For both meth- we normalized the same data to 100% for each plot ods of estimating cover, percentage cover can sum to and used canonical correspondence analysis (CCA) to [100% because plants in the various categories analyze and visualize the relationship of resident overlapped. We estimated plant diversity in each plot vegetation to treatments and location for 2007 and using the Shannon–Wiener diversity index (Peet 2008. Using the species vegetation data, we tested the 1974) and classified plants as native or introduced effects of location, treatment, and their interaction on according to USDA-NRCS (2010). the number of species, Shannon–Wiener diversity index, and number of native species per plot using Statistical analyses ANOVA. We used JMP 7.0 (SAS 2007) for ANOVA, ANCOVA, and survival analyses and XLSTAT We derived treatment means and variances from the (Addinsoft 2009) for CCA. eight replications of each treatment. We nested block within location, which we treated as a fixed effect. We used arc-sin square root transformation for Results proportions of V. rossicum emergence and survival. We used natural log transformations for analyses of Overall emergence, growth, and final biomass of shoot, root, and total biomass to achieve normally V. rossicum varied by location, disturbance treatment, distributed residuals. We used analysis of variance or the interaction of location and treatment (Table 1). (ANOVA) to test the fixed effects of location, Emergence was lowest in the herbicide-only and treatment, and their interaction on the proportion of herbicide ? tillage treatments at the plateau location seedlings emerging, the proportion surviving, shoot, (Fig. 1, Table 1). About 80% of plants that emerged root, and total biomass, plot diversity, and percentage did so by August 2007 (9 months after sowing), with of native species. We averaged individual plant some emergence continuing into October 2007 and biomass within each plot. We used analysis of through the 2008 growing season. Very few plants 123 70 Plant Ecol (2010) 211:65–77 emerged in 2009, the third growing season following 25 a sowing. At the hill top location, two seedlings (a) Plateau emerged in the mowed treatment and two emerged 20 in the herbicide-only treatment. At the plateau loca- 15 tion, one seedling emerged in the herbicide ? tillage b treatment. In plots that received herbicides, 12–14% 10 of emerging plants emerged by late May, whereas, in c control or mowed plots, less than 1% of plants had 5 c emerged by this time. This difference at the hill top location was no longer apparent at the end of the 0 experiment when total emergence did not differ 25 (b) Hill top a among treatments. Within each location, V. rossicum Emergence (%) a emergence in the herbicide-only and herbicide ? till- 20 ab ab age treatment plots did not differ (Fig. 1). For control 15 treatment plots, we observed the same percentage emergence at both locations. However, at the hill top 10 location, plots treated with herbicides had equal Control 5 Mowed emergence to the control plots (Fig. 1b). At the Herbicide-only Herbicide + tillage plateau location, emergence was greatest in the 0 mowed treatment plots and was lowest in the herbi- cide-only treatment plots (Fig. 1a). 29-May 10-Jul 20-Aug 2-Oct 8-May 17-Jun 1-Aug Results from Cox’s proportional hazards model, 2007 2008 showed that location, treatment, and the location by Fig. 1 Cumulative Vincetoxicum rossicum percentage emer- treatment interaction had no effect on the risk of gence (60 seeds sowed per plot) from May 2007 to August mortality over time. Furthermore, treatment and the 2008 after planting in November 2006 at two old field interaction of treatment with location did not affect locations. The same letters in the right-hand column indicate no significant differences among final emergence percentages percentage survival (Table 1). However, final per- within or between locations (LSD, P \ 0.05) (n = 8) centage survival of plants was greater at the hill top location (76 ± 3%) than at the plateau location number of plants with multiple stems (Fig. 2). (46 ± 5%) (Table 1). The percentage of plants with Furthermore, the survival of emerged individuals more than one stem (from polyembryonic seeds) was was also correlated with the number of polyembry- not different across locations or treatments or by the onic plants (slope = 1.6, R2 = 0.60, P \ 0.0001). interaction of location by treatment (P [ 0.05). Maximum stem lengths were greatest in the hill top However, the number of individuals that emerged herbicide treatments (Fig. 3, Table 1). The maximum within each plot was strongly correlated with the lengths of plants grown in the untreated control plots

Table 1 Results of ANOVAs (F values) for the fixed effects of location, treatment, and their interaction on Vincetoxicum rossicum emergence (all cohorts), survival to August 2008 of cohorts emerging prior to August 2007 and of all cohorts, maximum stem length in 2007 and 2008, and root, shoot, and total (root ? shoot) biomass Effect DF Emergence Emerg by August 2007 Overall 2007 2008 Shoot Root Total survival survival length length biomass biomass biomass

Location 1 29*** 22*** 33*** 101*** 57*** 54*** 19*** 21*** Treatment 3 5.4** 1.4 (ns) 2.7 (ns) 2.0 (ns) 11*** 31*** 13*** 14*** Location 9 treatment 3 9.0*** 2.1 (ns) 1.8 (ns) 25*** 6.4** 4.8** 1.5 (ns) 1.3 (ns) Data are from experimental establishment plots, where we examined the effects of a disturbance gradient in two old field habitats from 2007 to 2008 (n = 8) ** P \ 0.01, *** P \ 0.001 DF degrees of freedom, ns not significant 123 Plant Ecol (2010) 211:65–77 71

12 were similar across locations in 2007, but in 2008, Max. (a) Plateau maximum lengths at the hill top location (10 ± 2 cm) height 10 Control were 80% greater than at the plateau location Mowed bc Herbicide-only (6.1 ± 0.6 cm). Beginning in July 2007, treatment 8 Herbicide + tillage differences at the hill top location were clear, with cd greater growth in the herbicide treatments than in the 6 bcd control and mowed treatments (Fig. 3b). We observed 4 d the same pattern at the plateau location, but the only significant difference (by the end of the second 2 season) was that plants in the herbicide ? tillage 0 treatment had greater maximum lengths than plants in 16 (b) Hill top a the control treatment (Fig. 3a). Plants also had 61% Stem length (cm) 14 a more nodes per stem at the hill top location 12

(5.9 ± 0.3) than at the plateau location (3.6 ± 0.2) 10

(location effect, P \ 0.001). 8 Total biomass production per plant was several 6 bc times greater at the hill top location (0.24 ± 0.06 g) bcd 4 than the plateau location (0.05 ± 0.02 g) (Table 1). 2 Similarly, root biomass was greater at the hill top 0 location (0.16 ± 0.09 g) than the plateau location 30 May 10 Jul 20 Aug 3 Oct 8May 17Jun 1 Aug (0.04 ± 0.04 g) (Table 1). Plants from the herbicide 2007 2008 treatments had greater root and total biomass than Fig. 3 Vincetoxicum rossicum mean stem length per plot from plants from the control and mowed treatments May 2007 to August 2008 at 3-week intervals at two old field (Fig. 4, Table 1). The same pattern was generally locations under four levels of disturbance. The same letters in observed for shoot biomass within each location the right-hand column indicate no significant differences (Fig. 4, Table 1). ANCOVA results showed that the among maximum lengths within or between locations (LSD, P \ 0.05) (n = 8) ratio of root-to-shoot biomass did not vary across treatments. The root-to-shoot ratio at the plateau location (3.5 ± 0.2) was greater than at the hill top Vincetoxicum rossicum reproduction in this exper- location (2.6 ± 0.2). iment was minimal and was limited to the herbicide treatments at the hill top location. The production of too few flowers prevented us from performing statis- tical analyses. Of all reproducing plants in 2008, mean 30 follicle production was 6 ± 1 follicles plant-1. Flow- 25 ering plants had a minimum stem length of 30 cm.

20 Plants that flowered were more than twice as long (46 ± 2 cm) as the mean plant length (14.3 ± 0.7 cm) 15 for the same treatments in August 2008. All flowering

10 plants survived to the end of the study. y = 1.8 * x + 6.0 5 R² = 0.65 Number of seedlings emerged P < 0.0001 Competing vegetation 0 Competing vegetation overtopped the small V. rossi- 0246810 Number of polyembryonic individuals cum plants (data not shown). In the mowed treatment plots, other vegetation was shorter at the time of Fig. 2 Vincetoxicum rossicum emergence per plot as a assessment, a direct result of mowing annually to function of polyembryonic individuals per plot. Data were combined across four disturbance treatments and two old field 20 cm. Consequently, we found that light availability locations at ground level was higher in mowed plots (data not 123 72 Plant Ecol (2010) 211:65–77

0.2 a a plots more than the herbicide ? tillage treatment (a) Plateau (b) Hill top plots. In both years, we found Aster spp., Solidago 0.1 spp., and woody species primarily at the plateau b d cd bc bc bc location and Cyperus esculentus L. (yellow nutsedge) 0.0 B B only at the plateau location. We observed more 0.1 C. esculentus in plots that received herbicides (6 ± 2% cover) than in the mowed treatment plots Root 0.2 Shoot (0.10 ± 0.07% cover) and more plants in 2007 Biomass per plant (g) Root Shoot (7 ± 3% cover) than in 2008 (0.8 ± 0.4% cover). 0.3 A A Control plots had no C. esculentus plants. In both

Control Mowed Herb Herb + till Control Mowed Herb Herb + till years, G. mollugo was more dominant at the hill top than at the plateau location and regression analysis Fig. 4 Vincetoxicum rossicum root and shoot biomass at two showed that, at the plateau location, G. mollugo was old field locations across a disturbance gradient 2 years after sowing (Herb = herbicide-only; Herb ? till = herbicide ? negatively correlated with V. rossicum biomass tillage). For shoot biomass, bars with the same letters are not (P = 0.0003) (data not shown). significantly different within or between locations because the Vegetation diversity analyses using species rich- location by treatment interaction effect was significant (LSD, ness and the Shannon–Wiener diversity index gave P [ 0.05, n = 8). The location by treatment interaction effect was not significant for root or total biomass. Consequently, for largely the same results (Table 3), so only species root biomass, bars with the same letter (averaging across richness is plotted (Fig. 6). In 2008, 74 species were locations) are not significantly different (LSD, P [ 0.05) present at the plateau location and 59 were present at the hill top location. We observed 50% more species per plot at the plateau location (24.5 ± 0.7) than at shown). In 2007 (but not in 2008), cover of competing the hill top location (16.3 ± 0.7) (Table 3). We also resident vegetation was significant in explaining total observed 28% more species in the herbicide-treated V. rossicum biomass (Table 2). However, abundance plots (22.9 ± 0.9 species) than in the control and was not significant in explaining V. rossicum emer- mowed plots (17.9 ± 0.9 species). Percentage of gence or survival (data not shown). Competing native species did not differ among the treatments at vegetation abundance in 2007 was positively corre- the plateau location. In contrast, at the hill top lated with V. rossicum final biomass at the hill top location, we observed a higher percentage of natives location, but this was not apparent at the plateau in the more disturbed treatments than in the control location. The canonical correspondence analyses and mowed treatments (Fig. 6). (CCAs) indicated that the main effects of treatment and location significantly affected the composition of vegetation (Fig. 5). Two axes in the CCA accounted for over 90% of the data variation in both 2007 and Table 2 Results of ANCOVA (F values) for the fixed effects of location, treatment, and the location by treatment interaction 2008. In 2007, the F1 (x) axis variation mostly and the abundance of competing vegetation in 2007 and 2008 described the treatment effect and accounted for about as covariates on Vincetoxicum rossicum final total biomass 72% of the variation, while the F2 (y) axis described Effect DF Total biomass the location effect and explained about 19% of the variation (Fig. 5a). We observed the reverse trend in Location 1 21*** 2008, when location (on the x axis) explained 75% of Treatment 3 14*** the variation, whereas treatment (y axis) explained Location 9 treatment 3 2.4 (ns) about 18% of the variation (Fig. 5b). In 2007, we 2007 vegetation 1 4.2* found annuals almost exclusively in the herbicide 2008 vegetation 1 0.060 (ns) treatments, whereas we found perennial grasses and Data are from experimental establishment plots, where we broadleaf species almost exclusively in the mowed examined the effects of a disturbance gradient in two old field and control treatments. In contrast, annuals were habitats from 2007 to 2008 (n = 8) nearly absent in 2008. In 2008, the herbicide-only * P \ 0.05, *** P \ 0.001 treatment plots resembled the control and mowed DF degrees of freedom, ns not significant 123 Plant Ecol (2010) 211:65–77 73

1.2 Table 3 Results of ANOVAs (F values) for the fixed effects Hill top (a) 2007 of location, treatment, and their interaction on the number of 0.8 Gal species per plot, Shannon–Wiener diversity index, and number of native species per plot 0.4 AG Mowing Herb +till PG Effect DF Species/plot Diversity Native 0 Herb AB Control PB Location 1 126*** 120*** 41*** F2 (18.7 %) -0.4 Grn Treatment 3 17*** 8.4*** 3.2* -0.8 Location 9 treatment 3 1.8 (ns) 0.94 (ns) 3.3* Ast Categories Sdg Plateau Wdy Variables -1.2 Data are from Vincetoxicum rossicum experimental -1.5 -1 -0.5 0 0.5 1 1.5 establishment plots, where we examined the effects of a F1 (71.7 %) disturbance gradient in two old field habitats from 2007 to 2008 (n = 8) 2008 0.8 (b) * P \ 0.05, *** P \ 0.001 Wdy Control Ros DF degrees of freedom, ns not significant 04. Mowing Plateau Herb PG 0 Ast Grn Hill top Plateau Gal -0.4 PB 50 Hill top F2 (17.6 %) a -0.8 a ab ab Herb +till ab -1.2 Categories 40 Sdg Variables b -1.6 -1.5 -1 -0.5 0 0.5 1 1.5 c F1 (74.8 %) 30 c Fig. 5 Canonical correspondence analysis for Vincetoxicum rossicum experimental establishment plots across a disturbance 20

gradient at two old field locations, during the 2 years after Native species (%) treatments were established, a 2007; P \ 0.0001, Pseudo F = 4.1 and b 2008; P \ 0.0001, Pseudo F = 1.3 (Herb herbicide-only, Herb ? till herbicide ? tillage, AB annual 10 broadleaves, AG annual grasses, Ast upright Asteraceae spp., Gal Galium mollugo, Grn ground, PG perennial grasses, Ros creeping Rosaceae spp., Sdg yellow nutsedge, Cyperus 0 esculentus; Wdy woody species, PB other perennial Control Mowed Herb Herb + till broadleaves) Increasing Disturbance

Fig. 6 Percentage of native species in Vincetoxicum rossicum experimental establishment plots across a disturbance gradient Discussion (Herb herbicide-only, Herb ? till herbicide ? tillage). Data were collected from two old field locations in 2008, 2 years In this experiment, we found that V. rossicum demon- after treatments were established. Bars are means ? SE (n = 8). Bars with the same letter are not significantly strated high establishment success relative to reported different within and between locations (LSD, P \ 0.05) values of other old field species. We observed this result even in our undisturbed old field control Seeds that did not emerge in this experiment may treatments and at the location that was less suitable have remained in the seedbank. However, V. rossicum for V. rossicum establishment. Establishment and seeds likely have limited longevity in the seedbank, as survival rates of V. rossicum were higher than reported we observed low emergence in the second year (2008) for other old field plants co-occurring in these fields, and even lower emergence in the third year (2009). including S. altissima (1% establishment and sur- Additionally, seeds from the closely-related Apocy- vival in old field conditions) (Meyer and Schmid 1999) num cannabinum L. (hemp dogbane) have been and P. arundinacea (\10% establishment and survival reported to have almost no seed dormancy, with the in a wetland) (Lindig-Cisneros and Zedler 2002). majority of buried seeds germinating within one year

123 74 Plant Ecol (2010) 211:65–77 after sowing and germination below 1% after 4 years Aster and Solidago spp. (goldenrods) and more woody (Burnside et al. 1981). Thus, seeds that did not emerge species (Fig. 5), including Cornus racemosa Lam. in our experiment were probably lost due to a (grey dogwood) and Populus grandidentata Michx. combination of predation, decay, and movement to (bigtooth aspen) at this wetter site. Furthermore, the deeper soil depths, from where they would be unable plateau vegetation had not been mowed for 5 years, to emerge (Chambers and MacMahon 1994; Harper whereas the hill top vegetation was mowed the year 1977). before the experiment was initiated. Thus, the plateau location was at a later stage of secondary succession, Location differences which may have increased its resistance to V. rossicum establishment (Sheley and Krueger- The location and/or location by treatment interaction Mangold 2003). G. mollugo may also have limited effect was significant for all parameters we examined V. rossicum growth at the plateau location. We except embryonic status (Tables 1, 2, 3). Conditions observed a negative correlation between G. mollugo at the two locations differed substantially. At the cover and V. rossicum biomass at the plateau location. wetter plateau location in plots that received herbi- However, we observed no correlation between these cides, we observed standing water in some herbicide- species at the hill top location. Given that G. mollugo treated plots when we sowed V. rossicum. We also and V. rossicum have similar sprawling habits, observed more C. esculentus, a plant that usually perhaps they were in competition for the same niche occurs in wetlands (USDA-NRCS 2010), in herbicide- requirements at the wetter plateau location (Merse- treated plots than in the control and mowed plots and reau and DiTommaso 2003). only at the wetter plateau location. The wetter conditions at the plateau location may have been Disturbance intensity effects exacerbated by herbicide application, as the herbi- cides killed transpiring topgrowth of the resident Many invasive plants employ strategies to exploit vegetation, thereby reducing transpirational water loss disturbed sites that have high resource availabilities (Martin et al. 2003; Canham and Marks 1985). and low competition pressure (Davis et al. 2000; Furthermore, at the plateau location, we observed Orians 1986). We found that, although V. rossicum the greatest V. rossicum establishment in the mowing successfully established in all treatments, its pattern of treatment, where reduced light competition in combi- growth was strongly affected by the intensity of nation with intact vegetation likely provided more disturbance. At the hill top location, where V. rossicum suitable conditions for establishment than in the generally established well (Fig. 1), growth varied control plots. Thus, plants in the mowed plots had greatly across treatments. In herbicide-treated plots at the benefits of increased light availability, because we the hill top location, V. rossicum grew 2.4 times longer mowed annually, and lower competition for light than and over 10 times as large as plants in the less in the control plots. Furthermore, enough vegetation disturbed, and likely more competitive, control and remained in the mowed plots to dry out the soil, which mowed treatments (Figs. 3, 4). Reproduction was also likely created a more favorable root environment for only observed for plants in herbicide treatments. Thus, V. rossicum. Wet soil conditions may explain why we our results support the fluctuating resource hypothesis observed lower emergence, survival, and growth of of invasibility, which predicts that disturbance allows this species at the plateau location. Since soil moisture an increased susceptibility to invasion (Davis et al. status may be an abiotic factor that limits establish- 2000). Despite differing growth of V. rossicum plants ment of this invasive species, we would expect to find among treatments, survival was relatively high for all V. rossicum invading areas with soils that are treatments after the initial establishment period (until moderately well-drained or better drained. August 2007) (data not shown). The resident old field vegetation also differed We observed increased species richness in the between the two locations. The plateau location had a more severely disturbed treatment plots. Gibson et al. higher percentage of native species than the hill top (2005) also reported increased species richness in location (Fig. 6). In addition to finding C. esculentus response to disturbance. Grime (1973), and later only at the plateau location, we also observed more Connell (1978), proposed that species richness should 123 Plant Ecol (2010) 211:65–77 75 be highest at intermediate levels of disturbance. Given survival. Other work has shown that polyembryony that our herbicide treatments represent intermediate may confer no establishment or competitive advan- disturbances, our results support this prediction. tage (Blanchard et al. 2010; Hotchkiss et al. 2008). Consequently, the herbicide disturbance treat- Nonetheless, we suggest that polyembryony is a life ments in our experiment not only allowed greater history trait that increases the probability of propa- V. rossicum growth, but also enabled increased gule establishment regardless of the habitat distur- species richness. bance or locations in our experiment. In contrast to the relatively intact control and ‘‘Sit and wait’’ strategy mowed habitats, herbicide treatments created the conditions necessary for rapid growth and reproduc- Vincetoxicum rossicum plants appeared to employ a tion. In this experiment, herbicide treatments coin- ‘‘sit and wait’’ or lag phase strategy when conditions cided with the V. rossicum establishment phase. Light were unsuitable for growth and reproduction. Condi- and space availabilities were likely greater in herbi- tions were less suitable in our control and mowed cide treatments than in control and mowed treat- treatments and, generally at the plateau location. The ments. Therefore, in addition to establishing in intact higher root-to-shoot ratio of V. rossicum at the communities and tolerating periods of low resource plateau location further reflects this allocation strat- availability, V. rossicum demonstrated an opportu- egy. We have observed seedling-like V. rossicum nistic use of resources by growing longer and larger juveniles in old field and forest habitats in NY State when more resources were available (Figs. 3, 4). and, based on root crown anatomy, have determined Findings from other studies have demonstrated that that this juvenile stage may last for several years V. rossicum can additionally exhibit a relatively high (personal observations, KMA, AD, LRM). Greenberg competitive ability (Blanchard et al. 2010; Smith et al. (2001) identified such a ‘‘sit and wait strategy’’ et al. 2006). Thus, V. rossicum seems to have the in Celastrus orbiculatus Thunb. (Oriental bitter- ability to tolerate competition and compete for sweet), another shade-tolerant, non-native invasive resources, thus being able to overcome various vine that grows rapidly in response to disturbance. A establishment constraints (Goldberg and Landa prolonged juvenile stage characterized by slow 1991; Grime 1977; Gurvich et al. 2005). growth allows more resources to be allocated to At the plot level, we noted lower V. rossicum belowground structures until energy reserves and establishment where perennial grass cover (e.g., conditions are suitable for rapid growth and repro- Elymus repens, P. arundinacea, Phleum pratense, duction. V. rossicum likely needs to accumulate a and P. pratensis) was relatively high, suggesting that threshold stem length or level of biomass before dense grass may resist establishment of this species producing seeds and contributing to population (see Barthram et al. 2005). Maintaining perennial expansion, the next phase in invasion. The ‘‘sit and grasses before invasion by V. rossicum may contrib- wait’’ strategy is not unique to invasive species. For ute to biotic resistance against this species by example, Acer saccharum Marsh. (sugar maple) is a decreasing habitat invasibility (Elton 1958; Levine stress-tolerant native forest tree species capable of et al. 2004; Prober et al. 2005; von Holle et al. 2003; surviving for decades as saplings in the forest Sheley and Krueger-Mangold 2003). Similarly, understory (Canham 1985). Nonetheless, it is impor- perennial grasses may be ideal restoration species tant to recognize that a ‘‘sit and wait’’ strategy is one following V. rossicum eradication. mechanism that allows invasive species to penetrate Future research could assess V. rossicum emer- highly competitive habitats. gence and survival across moisture and light gradi- A characteristic of V. rossicum that likely contrib- ents. Based on the results of our experiment, we utes to its invasiveness is polyembryony, a condition propose the following testable hypotheses: V. rossi- in which multiple embryos are present in a single cum performance (emergence, growth, and survival) seed. Ladd and Cappuccino (2005) found that poly- (1) will increase with soil drainage and (2) will embryony increased the probability of at least one increase with habitat light availability; finally, (3) seedling surviving per seed. We found that polyem- yearly mowing will increase V. rossicum establish- bryony allowed increased emergence (Fig. 2) and ment success. 123 76 Plant Ecol (2010) 211:65–77

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