Survival, Growth and Gas Exchange of Celastrus Orbiculatus Seedlings in Sun and Shade

Am. Midl. Nat. 151:233–240

Survival, Growth and Gas Exchange of Celastrus orbiculatus Seedlings in Sun and Shade

1 JOSHUA W. ELLSWORTH, ROBIN A. HARRINGTON AND JAMES H. FOWNES Department of Natural Resources Conservation, University of Massachusetts, Amherst 01003

ABSTRACT.—The invasive vine Celastrus orbiculatus Thunb. (Oriental bittersweet) dominates gap and edge environments, but may also colonize undisturbed forest. We compared survival and growth of C. orbiculatus seedlings in ﬁeld plots under 2%, 28% and 100% sun. From transplanting through the ﬁrst autumn, survival and growth did not differ among treatments. In the second growing season, survival at 2% sun was 76%, compared to 96% in 28% sun. Growth and biomass were greater in the 100% and 28% sun treatments than 2% sun. The ratio of leaf to total biomass (LBR) decreased with shade, but leaf mass per leaf area (LMA) decreased proportionally more, so that the leaf area per unit biomass (LAR) increased in the shade. Photosynthesis, stomatal conductance and the ratio of photosynthesis to conductance (A/g) decreased in the shade. The ability of C. orbiculatus to survive under deep shade despite its slow growth implies that intact forests are vulnerable to invasion and that established understory populations should be controlled before harvesting or thinning the forest.

INTRODUCTION Celastrus orbiculatus Thunb. (Oriental bittersweet) is one of many introduced plant species threatening native forest ecosystems in the eastern U.S. (Dreyer et al., 1987; McNab and Meeker, 1987; Robertson et al., 1994). Once established, C. orbiculatus can overtop and girdle native trees and shrubs along roads, in clearings and in forest gaps (Patterson, 1974; Dreyer et al., 1987; McNab and Meeker, 1987). The success of C. orbiculatus may be due to frequent natural and human-caused disturbances in the eastern U.S. (Robertson et al., 1994; Luken et al., 1997; McDonnell et al., 1997; McNab and Loftis, 2002). Disturbances can lead to plant invasions through an increase in the availability of resources such as germination sites, light and water (Hobbs and Huenneke, 1992; Greenberg et al., 2001). However, it has also been suggested that C. orbiculatus seedlings can become established and survive in intact forest understory (Patterson, 1974, 1975; Greenberg et al., 2001). This ability has important implications for forest management because disturbances that result in increases in light may release C. orbiculatus already established in the understory. The objectives of this study were: (1) to determine whether C. orbiculatus can survive as seedlings in deep shade, deﬁned as 2% of incident light (Walters and Reich, 1996), (2) to determine what mechanisms enable its survival and (3) to assess how growth and survival differ in response to deep shade, moderate shade and full sun. The occurrence of Celastrus orbiculatus as seedlings in the understory does not mean that a seedling bank is an important part of its life history or invasion process: ongoing seed rain and germination may be followed by seedling mortality. Long-term survival, slow growth until release and more rapid growth following release characterize a true seedling bank (Marks and Gardescu, 1998). Although some species have survived for many years in the seedling bank (Marks and Gardescu, 1998), previous studies tracking C. orbiculatus growth and survival in response to light have been restricted to a few months (Patterson, 1974, 1975;

1 Corresponding author: Telephone: (413) 577 0204; FAX: (413) 545 4358; e-mail: rharring@ forwild.umass.edu

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Greenberg et al., 2001). The distinction is important because the build-up of a seedling bank over many seed cohorts would allow a species to dominate a site more quickly following release than if most seedlings died each year in the understory. It is sometimes assumed that growth rate represents ‘‘vigor’’ and, hence, whole plant carbon balance, but growth in the shade may not correlate with survival in the shade (Walters and Reich, 1999). In comparisons among species, growth in shade was higher, but survival was lower for intolerant vs. tolerant trees (Kitajima, 1994; Pacala et al., 1996). Shade tolerant species invested less in leaf biomass (i.e., had lower ratio of leaf biomass to total, or LBR) than intolerant species when grown in low light (Walters and Reich, 1999). Within a species, reduction in LBR due to shade may be offset by decreasing leaf mass per unit leaf area (LMA). The ratio of leaf area to total (aboveground) biomass (leaf area ratio, or LAR) is an index of light capture vs. respiratory costs and its maintenance or increase in the shade is one mechanism by which plants adjust to the shade environment (Givnish, 1988). The invasive Sapium sebiferum had a greater range in LMA and LAR than the native Fraxinus caroliniana, which partly explained its greater growth at low light ( Jones and McLeod, 1990). We hypothesized that if Celastrus orbiculatus seedlings survived deep shade for a full year their LAR would be equal to, or greater than, plants in moderate shade or full sun. Conversely, if they did not survive well, we predicted that either net photosynthesis at ambient light levels would be close to zero or that LAR would be decreased in deep shade. We used shade structures to control light levels in ﬁeld plots of Celastrus orbiculatus. Although the quality and distribution of light under shade cloth differs from that in understories and gaps (Wayne and Bazzaz, 1993; Lee et al., 1996), we wanted to avoid confounding decreased light with decreased water or nutrient availability, conditions that can co-limit plant growth in actual forest understories (Shirley, 1945; Walters and Reich, 1996). In addition to the 2% and full sunlight treatments, we used a moderate shade treatment of 28% to determine whether C. orbiculatus would reach its growth potential in light levels approximately equivalent to a small canopy opening or thinned canopy, as well as to assess whether any lack of response in the full sunlight treatment might be attributed to water stress or other factors. To supplement these interpretations, we measured foliar d13C, which provides an integrated estimate of the ratio of photosynthesis to conductance (Farquhar and Richards, 1984) and instantaneous gas exchange under ambient conditions.

METHODS Site and seedling preparation.—Plots were located in an open grassy field receiving full exposure to sun. Soils are classified as Sudbury fine sandy loam (Sandy mixed mesic Aquic Dystrochrepts). Prior to planting, the soil was tilled in mid-June and again in mid-July to remove existing vegetation. We collected fruits from vines in April 2000, air-dried them and removed the seeds from the fleshy fruit. Seeds were placed in water and floating ones discarded. The remaining seeds were cleaned with mild bleach solution and planted 5 mm deep in 10 cm 3 10 cm pots of peat and perlite potting mix. Pots were placed in the shade of a hemlock tree (5–10% full sun) and kept well watered. Seedlings were planted in field plots on 26 July (day 56), when they had two true leaves. Seedling size at planting averaged 0.04 m (SD ¼ 0.004). Experimental design and implementation.—The three treatments (2%, 28% and 100% sunlight) were replicated in four blocks for a total of 12 plots. Each plot was 3 3 3 m and 26 seedlings were planted in each plot. Wooden frames 1.2 m in height were covered on the top and all four sides with one layer of 72% woven shade cloth (American Clayworks, Denver, Colo.) for the 28% sun treatment and 3 layers of 72% woven shade cloth for the 2% sun treatment. Light levels were verified by measurements with a quantum sensor (LI-190S13, 2004 ELLSWORTH ET AL.: SURVIVAL OF CELASTRUS 235

LI-COR, Lincoln, Nebr.). No frame was placed over the 100% sun treatment. Seedlings were planted out with additional potting soil mixed into the hole to promote hydraulic continuity with the ﬁeld soil. Seedlings were watered upon planting; the adequate rainfall during summer 2000 made further watering unnecessary. Plots were weeded three times in summer and fall 2000. Because of rapid weed growth during the ﬁrst summer, we laid down Weedblock 3þ weed barrier fabric to all plots in the spring of 2001. Herbivory (most likely by rabbits and voles) was observed in all plots during the 2000 growing season and winter of 2000/2001 and, by spring 2001, had removed essentially all new growth. Therefore, we added a strip of chicken wire to the base of the shade houses and fenced the 100% sun plots with 3-foot high chicken wire in April 2001. We watered plots every 2 or 3 d in early May 2001 and late August 2001 due to unusually dry weather. Measurements.—We measured stem length of each seedling during the 2000 growing season. However, in spring 2001 the vines branched and multiple shoots grew out. Thereafter, we measured the total living length (TLL) of stems on each plant. In September 2001, we harvested all plants, divided aboveground biomass into leaves and stems and measured leaf area with a LI-COR LI-3100 area meter. Leaves and stems were oven dried at 70 C and weighed. Leaf weight per leaf area (LMA, g m2), the ratio of leaf biomass to total aboveground plant biomass (LBR) and ratio of leaf area to total aboveground plant biomass (LAR, m2 kg1) were calculated for each plant from the harvest data. Plot variables were calculated as the mean of individual plant values. Leaf samples were pooled by plot and analyzed for nutrient content by the University of Massachusetts Soil and Plant Analysis Laboratory. Pooled leaf samples were also analyzed for carbon isotope composition (d13C) at the University of Georgia Stable Isotope Lab. During the week prior to harvest, midday CO2 assimilation at ambient light levels was measured with a portable CIRAS 1 photosynthesis system (PP Systems, Amesbury, Mass.) using a broadleaf cuvette. Measurements were made on one fully expanded leaf per plot. Leaves were maintained in their natural orientation during measurements. Data analysis.—Survival was calculated for three intervals: from planting until October 2000 (transplant), from October 2000 through May 2001 (over winter) and from May through September 2001 (growing season). Survival for each interval and cumulative for the experiment were arcsine-square root transformed for analysis. Plot means for growth and biomass measurements were log transformed to homogenize variance among treatments. We present means and standard deviations calculated from untransformed data. The statistical model was a randomized block analysis of variance with the following sources of variation (and degrees of freedom): treatment (2), block (3), treatment 3 block (error) (6), followed by means separation using Tukey’s HSD Test. Linear regression was used to evaluate correlation between traits.

RESULTS Survival, growth and allocation.—Survival following planting ranged from 87% to 96% and did not differ among treatments (Table 1). Over-winter survival was lower than during the other intervals and was lower in the 100% sun treatment than the others. Browsing during the fall and winter, and a late frost the following spring, may have caused mortality. Survival during the growing season was lowest in the 2% sun treatment, but at 76% it was still relatively high. Cumulative survival did not differ among treatments, although it was somewhat higher in the 28% sun (Table 1). Vine growth from transplanting through fall 2000 averaged 0.08 m (SD ¼ 0.04 m) and did not differ signiﬁcantly among treatments because of high variability and the relatively short growing period (83 d). Most of this 236 THE AMERICAN MIDLAND NATURALIST 151(2)

TABLE 1.—Mean (n ¼ 4) survival of Celastrus orbiculatus seedlings following planting in 2000, over winter 2000–2001, during the 2001 growing season and cumulative survival from planting in 2000 to the end of the growing season in 2001. Means with the same letter are not signiﬁcantly different among treatments (P , 0.05). Standard deviations are in parentheses

Treatment Transplant Winter Growing season Cumulative (% sun) survival (%) survival (%) survival (%) survival (%) 100 96 (3) 49 (21)b 90 (9)ab 43 (20) 28 87 (19) 84 (12)a 96 (4)a 70 (21) 2 94 (7) 60 (12)ab 76 (5)b 43 (11) P value ns 0.031 0.029 ns growth was lost to herbivory in late fall or winter, but, because treatments did not differ in growth, they also did not differ in herbivory. During the 2001 growing season, TLL growth and TLL at harvest were an order of magnitude lower in 2% sun than the other treatments, but the 28% and 100% sun treatments did not differ (Table 2). Leaf, stem and total aboveground biomass followed the same pattern (Table 2). Therefore, seedlings at 2% sun decreased in growth much more than in survival. LMA and LBR decreased in deep shade whereas LAR increased (Table 3). The relative magnitude of the difference in LMA was much greater than that of LBR, indicating that plasticity in leaf morphology was sufﬁcient to adjust to 2% of full sunlight. Leaf characteristics and gas exchange.—Foliar N concentration was higher in the 2% sun than in the other treatments (Table 4). d13C increased (i.e., became less negative) with increased light levels (Table 4), suggesting that the long-term ratio of assimilation (A) to stomatal conductance (g) was higher. The instantaneous gas exchange measurements at ambient light levels indicate that increased A/g ratio occurred because of higher photosynthesis in the light, not because of stomatal closure in the full sun (Table 4). Although the 100% sun had higher water-use efﬁciency, we did not see evidence of drought stress.

DISCUSSION The rapid growth rates of Celastrus orbiculatus in full and partial sun demonstrate the aggressive potential of this invasive vine species. By comparison, sprouts of Populus grandidentata grow 0.9 to 1.8 m in the ﬁrst year (Laidly, 1990) and sprouts of Liriodendron tulipifera can average 1.4 m per year (Beck, 1990). Seedlings of C. orbiculatus did not grow much in 2% sun, but their relatively high survival of 40% over 14 mo is comparable to the shade-tolerant trees Acer saccharum and Ostrya virginiana, which had approximately 20%

TABLE 2.—Mean (n ¼ 4) total living shoot length (TLL) growth during the second growing season, TLL at the time of harvest, leaf mass, stem mass and total aboveground mass at harvest. Means with the same letter are not signiﬁcantly different among treatments (P , 0.05). Standard deviations are in parentheses

Treatment TLL growth Final TLL Leaf mass Stem mass Aboveground mass (% sun) (m) (m) (g) (g) (g) 100 2.0 (0.9)a 2.1 (0.9)a 6.0 (3.0)a 4.2 (2.2)a 9.9 (5.6)a 28 4.6 (3.4)a 4.7 (3.4)a 7.1 (5.7)a 7.3 (6.4)a 14.4 (11.9)a 2 0.17 (0.03)b 0.22 (0.03)b 0.16 (0.06)b 0.16 (0.05)b 0.33 (0.11)b P value 0.0002 0.0003 0.0001 0.0003 0.0002 2004 ELLSWORTH ET AL.: SURVIVAL OF CELASTRUS 237

TABLE 3.—Mean (n ¼ 4) leaf mass per unit leaf area (LMA), leaf area ratio (LAR) and leaf biomass ratio (LBR) for Celastrus orbiculatus seedlings at the end of two growing seasons. Means with the same letter are not signiﬁcantly different (P , 0.05). Standard deviations are in parentheses

Treatment (% sun) LMA (g/m2) LAR (m2/kg) LBR 100 58 (4)a 10.9 (0.1)a 0.58 (0.05)a 28 34 (3)b 15.9 (0.1)b 0.53 (0.03)ab 2 22 (2)c 24.8 (0.4)c 0.48 (0.04)b P value ,0.0001 ,0.0001 0.0498

survival over 2 y when grown in shade houses at 2% sun (Walters and Reich, 1996). In a 23-y study of A. saccharum seedlings in forest understory, annual survival of the original cohort averaged over 90% per year, while newer cohorts had 63% survival in their first year (Marks and Gardescu, 1998). Our results show that Celastrus orbiculatus responds to deep shade through leaf-level and whole plant responses. Its leaves were able to make morphological adjustments to low light and photosynthesize at low light levels, which agrees with previous findings (Patterson, 1975). Despite reduced allocation to leaf biomass in the 2% light treatment, C. orbiculatus was able to reduce its LMA by 60% relative to that in full sun, resulting in an increase in LAR. This result is consistent with another study comparing survival and growth of native and alien woody plants in open vs. understory plots: all species had somewhat lower LBR in the understory, but those that maintained LAR generally had higher understory survival (Sanford et al., 2003). Other factors may affect survival in the understory as well, such as allocation to roots and carbon storage (Kobe, 1997). The 28% and 100% sun treatments did not differ significantly in growth (Table 2), but there was a trend towards higher growth in the 28% treatment. This observation suggests that stress or injury was less severe in the 28% sun treatment. The decrease in foliar d13Cin the 100% sun treatment indicates that water-use efficiency was higher in that treatment, but the gas exchange measurements do not support the hypothesis that this difference arose from water stress; rather, photosynthesis increased in full sun. It is possible that more frequent gas exchange measurements might have detected stomatal closure at other times in the growing season. The variation in foliar N appears to be a dilution effect, but the concentrations are relatively high (above 3.0%) and do not appear to indicate N deficiency. The use of shade cloth to vary light levels may have influenced the results in both expected and unexpected ways. In forest understories, light, water and nutrients may be simultaneously reduced compared to openings (Shirley, 1945; Walters and Reich, 1996; Lusk et al., 1997), so artificial shade is not intended to completely simulate the understory environment. Further- more, the spectral distribution and spatial and temporal dynamics of light in the understory are not duplicated by shade cloth (Wayne and Bazzaz, 1993; Lee et al., 1996). An unintended effect of the shade houses was that they protected plants from a late spring frost in May 2001. Overstory canopy cover reduces frost damage (Smith, 1986, p. 203) and we observed some shoot dieback in the uncovered 100% sun treatment. This frost event may partly account for the high variation in winter survival rates (Table 1) and the somewhat lower mean growth in the 100% sun treatment (Table 2). The benefits of using shade cloth were that the effect of light was not confounded with water and nutrient availability and the light environment was relatively simple to characterize compared to the extremely dynamic understory light regime. An unanticipated factor in our study was herbivory after planting and through the winter. The effects did not differ among treatments, so our conclusions are not vitiated by this 238 THE AMERICAN MIDLAND NATURALIST 151(2)

2 1 2 1 TABLE 4.—Assimilation rate (A, lmol CO2 m s ), stomatal conductance (g, mmol m s ), A/g (lmol mmol1), foliar d13C, and foliar nitrogen (N) concentration (%) of Celastrus orbiculatus seedlings grown under three different light levels. Standard deviations are in parentheses. Means with the same letter are not signiﬁcantly different among treatments (P , 0.05)

Treatment (% sun) A g A/g d13C Foliar N 100 14.3 (3.2)a 277 (131)ab 57 (17)a 28.4 (0.5)a 3.18 (0.24)b 28 7.9 (2.1)b 289 (33)a 27 (6)b 31.1 (1.0)b 3.42 (0.2)b 2 1.2 (0.4)c 99 (26)b 13 (6)b 33.8 (0.3)c 3.80 (0.09)a P value 0.0001 0.0318 0.0042 0.0001 0.0038 disturbance, but care should be taken in extrapolating the growth and survival rates to new situations. Small mammal predation on seeds and seedlings has been shown to have major effects on vegetation composition in openings (Gill and Marks, 1991; Ostfeld et al., 1997). Inter-speciﬁc variation in susceptibility and response to herbivory may inﬂuence the success of invading woody and herbaceous plant species relative to sympatric native species (Caldwell et al., 1981; Luken and Mattimoro, 1991; Schierenbeck et al., 1994). The impact of herbivory on Celastrus orbiculatus seedlings, combined with their high survival in shade, implies that small mammals may play an important role in limiting the establishment of a seedling bank population in this species. This control on plant invasions deserves further study. In summary, our results suggest that if Celastrus orbiculatus seedlings have become established in dense forest understories, a relatively high proportion of seedlings can survive at light levels that are as low as 2% of full sun. Plasticity in leaf-level and whole-plant characteristics allow C. orbiculatus to act like a shade-tolerant species in low light and a fast- growing species in high light. Growing in full or partial sun, C. orbiculatus plants may be able to overtop 1–2 m tall vegetation by the end of one full growing season. The ability to establish a seedling bank in undisturbed forest suggests that high priority sites for conservation are at risk whenever a seed source is nearby. The existence of a seedling bank, and the ability to grow rapidly in response to moderate light increases, implies that C. orbiculatus in the understory should be eradicated before thinning, selective timber harvests or road construction begins. To our knowledge, there is no documentation of the economic cost of failure to control understory populations of C. orbiculatus. Our results, and the many observations of its aggressive growth and domination of openings (Patterson, 1974; Dreyer et al., 1987; McNab and Meeker, 1987), suggest that failure to control it would result in severe forest degradation and considerably higher future costs associated with forest restoration.

Acknowledgments.—This research was supported by the U.S.D.A. N.R.I. Competitive Research Grants Program (award number 00-35320-9089), the Cooperative State Research Extension, Education Service, U.S.D.A., Massachusetts Agricultural Experiment Station, under Project No. 6-35889, and the Northeast Center for Urban and Community Forestry, USDA Forest Service. We thank T. Cassidy, L. Davis, J. Gaviria, L. Knapp, D. Pepin, N. Sanford and K. Turner for assistance in all stages of the experiment.

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SUBMITTED 17 MARCH 2003 ACCEPTED 15 SEPTEMBER 2003