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Seedling emergence, growth, and allocation of Oriental bittersweet: effects of seed input, seed bank, and forest floor litter
Forest Ecology and Management 190 (2004) 255–264
Seedling emergence, growth, and allocation of Oriental bittersweet: effects of seed input, seed bank, and forest floor litter Joshua W. Ellsworth, Robin A. Harrington*, James H. Fownes Department of Natural Resources Conservation, University of Massachusetts at Amherst, Amherst, MA 01003, USA Received 28 July 2003; received in revised form 24 September 2003; accepted 12 October 2003
Abstract The establishment of invasive plant populations is controlled by seed input, survival in the soil seed bank, and effects of soil surface disturbance on emergence, growth, and survival. We studied the invasive vine Celastrus orbiculatus Thunb. (Oriental bittersweet) to determine if seedlings in forest understory germinate from the seed bank or from seed rain. We also conducted a greenhouse experiment to investigate the role of leaf litter mass and physical texture on seedling survival, growth, and allocation. In the understory of an invaded mixed hardwood forest, we measured seed input, seedling emergence with seed rain, and seedling emergence without seed rain. Mean seed rain was 168 seeds m2: mean seedling emergence was 107 m2, and there was a strong correlation between seed rain and seedling emergence. The ratio of seedlings to seed input (0.61) was close to the seed viability (0.66) leaving very few seeds to enter the seed bank. Seed bank germination under field conditions was low (1 seedling m2). Soil cores were incubated in a greenhouse to determine seed bank viability, and germination from these soil cores did not occur. To determine how litter affects seedling establishment and growth, we measured seedling emergence and biomass allocation in a greenhouse experiment. Seeds were placed below intact and fragmented deciduous leaf litter in amounts ranging from zero to the equivalent of 16 Mg ha1. Seedling emergence was not affected by fragmented litter, but decreased to <20% as intact litter increased to 16 Mg ha1. Increasing litter resulted in greater allocation to hypocotyl and less to cotyledon and radicle, and this effect was greater in intact litter. C. orbiculatus seedlings achieve emergence through forest floor litter through plasticity in allocation to hypocotyl growth. The low survival of C. orbiculatus in the seed bank suggests that eradication of seedling advance regeneration and adult plants prior to seed rain may be an effective control strategy. However, the intact forest floor litter of an undisturbed forest will not prevent seedling establishment. # 2003 Elsevier B.V. All rights reserved. Keywords: Celastrus orbiculatus; Forest understory; Invasive species; Seed rain
1. Introduction Plant invasions are often associated with disturbances (e.g. Mazia et al., 2001; McNab and Loftis, *
Corresponding author. Tel.: þ1-413-577-0204; fax: þ1-413-545-4358. E-mail address: [email protected] (R.A. Harrington).
2002), but several non-native woody species have successfully invaded relatively undisturbed forests (Luken, 1988; Harrington et al., 1989; Webb and Kaunzinger, 1993; Woods, 1993; Cassidy et al., in press). Although shade and nutrient availability may limit the growth of invaders once they are established (Cassidy et al., in press; Sanford et al., 2003; Ellsworth et al., in press), the fates of seeds and seedlings
0378-1127/$ – see front matter # 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2003.10.015
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determine establishment in the understory and therefore have important implications for forest management. If enough seeds germinate and survive, then populations can establish that may grow slowly but respond rapidly to release by canopy opening (Greenberg et al., 2001). Conversely, if seeds remain viable in the soil, they can accumulate into a seed bank that is capable of response to soil disturbance (Paynter et al., 1998). In this case, survival in the soil seed bank and how soil surface disturbance affects emergence, growth, and survival are key controls on the establishment of invader populations. The purpose of this research was to determine whether Celastrus orbiculatus Thunb. (Oriental bittersweet), an invasive woody vine from eastern Asia, forms a seed bank and how forest floor disturbance affects its germination, growth and seedling survival. Seeds of C. orbiculatus mature in autumn and are dispersed by birds and mammals throughout the fall, winter and early spring (Patterson, 1974; Greenberg et al., 2001; Silveri et al., 2001). It is not clear whether seeds of C. orbiculatus can remain dormant in the seed bank. Seed bank longevity varies widely between species (Roberts, 1981; Thompson, 1987; Simpson et al., 1989), ranging from transient seed banks, where seeds persist only through the summer, to persistent seed banks, where viable seeds can last for decades (Thompson and Grime, 1979; Baskin and Baskin, 1989). If a species’ seeds persist in the seed bank, delayed germination may be triggered by natural or human-caused disturbances, such as logging or road building, that turn the soil or increase light levels at the forest floor (Livingston and Leck, 1968; Thompson, 1987; Baskin and Baskin, 1989; Ricard and Messier, 1996). Furthermore, control programs timed to kill seed-bearing plants prior to fruit maturation may stop the dispersal of a new seed crop, but do not ensure that dormant seeds present on site would not germinate in the future. Although some land managers report that C. orbiculatus seeds persist in the seed bank (The Nature Conservancy Connecticut Chapter, 2002), a 2-year experiment in a greenhouse did not detect germination after 1 year (Kostel-Hughes et al., 1998a). Many seed bank species have small seeds, often less than 2 or 3 mg (Pickett and McDonnell, 1989), which may decrease detection by seed predators (Thompson, 1987). By contrast, C. orbiculatus seeds weigh
10–12 mg (Patterson, 1974; our observations). Larger-seeded species that persist in the seed bank, such as Prunus pensylvanica (pin cherry), have thick seed coats (Wendel, 1990). Unlike P. pensylvanica, however, C. orbiculatus does not require mechanical or chemical scarification prior to germination (Patterson, 1974; Greenberg et al., 2001; our observations), suggesting that its seed coat is not sufficiently thick to protect it through multiple years of burial in the soil. Therefore, we hypothesized that C. orbiculatus would not persist in the seed bank, and that the previous year’s seed rain is the main source of seedling recruits. Forest floor litter decreases germination and seedling emergence through shading, biochemical effects, and physical obstruction to the emergence of a seed’s cotyledons and radicle (Sydes and Grime, 1981a; Facelli and Pickett, 1991a; Guzman-Grajales and Walker, 1991; Molofsky and Augspurger, 1992). Physical obstruction may either prevent seedling emergence or force seedlings to allocate more stored energy to hypocotyl growth in order to penetrate the litter layer, leaving less energy for allocation to the radicle and cotyledons. Such changes in allocation result in spindly, less sturdy seedlings with reduced ability to capture light, water, and nutrients (Facelli and Pickett, 1991a,b; Peterson and Facelli, 1992). Litter texture may also influence establishment, with coarse litter being more difficult to penetrate than fine litter (Peterson and Facelli, 1992). Many plant species require disturbances of the soil surface or organic litter layer in order to become established, in part because of the barrier posed by leaf litter (Keever, 1973; Marks, 1983; Facelli and Pickett, 1991a). Surveys of forest tracts show that C. orbiculatus is more common along logging roads (Silveri et al., 2001) and in areas that experience soil and litter disturbance from logging, windthrow, and foraging wildlife (McNab and Loftis, 2002). Litterlayer mass also varies naturally locally (Sydes and Grime, 1981b) and over time due to seasonal fluxes in decomposition rates and input (Facelli and Pickett, 1991a). Seasonal fluctuations in litter-layer mass are especially pertinent to C. orbiculatus because fruits mature in late September and can remain on the vine through the winter. Thus, viable seeds are dispersed into a wide range of natural litter conditions. We hypothesized that the emergence success of C. orbiculatus would decrease with increasing litter mass and
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that successful establishment of C. orbiculatus seeds would be greater when seeds were placed below fragmented litter rather than equal amounts of intact litter. We also hypothesized that increasing litter mass and coarseness would cause C. orbiculatus seedlings to allocate more to hypocotyls and therefore less to cotyledons and radicles.
the spring and summer of 2001 as a measure of germination from seeds that had been dormant for 1 year. One year later, in 2002, eight exclosures were still intact and were examined in mid-June for any further seedling recruitment. Seedlings were distinguished from root sprouts by the presence of cotyledons.
2. Methods
2.3. Experiment I: seedling recruitment from seed rain
2.1. Site description We conducted both field and greenhouse experiments to investigate factors that influence C. orbiculatus establishment. The source population was a dense population of fruit-producing C. orbiculatus vines in the canopy of a young, mixed-deciduous stand in the Sylvan Woods of the Waugh Arboretum, University of Massachusetts, Amherst. Dominant canopy-tree species included northern red oak (Quercus rubra), hickory (Carya spp.), and red maple (Acer rubrum), and the shrub layer was dominated by honeysuckle (Lonicera spp.).
Seed rain from the 2000 seed crop was estimated from seeds trapped by the exclosures in subplot 1 (Section 2.2). We collected seeds from the traps in May 2001. In subplot 2, a frame covered only with 6 mm wide mesh allowed C. orbiculatus seeds from seed rain to enter the soil, but protected them from herbivory. Seedlings were counted during the summer of 2001. The ratio of seedlings recruited to seed input was estimated from the slope of the geometric mean regression (GMR) between numbers of seedlings and number of seeds in paired subplots (Krebs, 1999, p. 559). Survival of seedlings under the frames was measured through August 2001.
2.2. Experiment I: seedling recruitment from seed bank
2.4. Experiment I: viability of seed rain and seed bank
To assess the potential importance of a seed bank to seedling recruitment, we experimentally compared seedling recruitment in 2001 with and without seed rain from the 2000 growing season. In the fall of 2000 (before seed rain), we selected 15 sampling locations beneath the vine canopy. At each we laid out four 61 cm 61 cm (0.37 m2) subplots. The subplots at each site were used to measure three variables: (1) seed bank germination in field conditions, (2) seed bank germination in greenhouse conditions (viability of the seed bank), and (3) the proportion of seed rain that germinated the first year after dispersal. Seedling recruitment from the seed bank was estimated from subplot 1 using exclosures that prevented the 2000 seed crop from reaching the soil. Exclosures were wooden frames covered with 2 mm screen to catch seed. A second frame with 6 mm wire mesh was placed on top of the fine screen to protect fruits and seeds from animal consumption. Seedlings recruiting under the mesh were tagged and counted throughout
We assessed viability of seeds in seed rain by collecting C. orbiculatus fruits from vines in April 2000, air-drying them for 30 days and removing the seeds. One hundred and forty-three seeds were kept moist for 41 days at 18 8C and checked for germination success. The 95% confidence limits for the proportion of viable seeds was calculated using a binomial distribution (Krebs, 1999, p. 270). Seed bank viability was tested in greenhouse conditions. Five subsamples of the A soil horizon were collected in mid-October 2000 from the subplot 3 at each location using a 7 cm diameter bulb planter. The five subsamples were pooled and stored in plastic bags at 4 8C. for 80 days. Each sample was then spread out to a depth of less than 1.75 cm on top of potting soil in flats and placed in greenhouse with ambient light measuring 40% of full sun. Flats were well watered. The emergence of C. orbiculatus seedlings was monitored for 60 days. We also collected soil cores from the subplot 4 in early fall 2001 to assess if seeds from
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the 2000 seed rain remained viable in the seed bank. The collection and germination methods followed those in the previous greenhouse study. 2.5. Experiment II: response to litter amount and texture We conducted a greenhouse study to examine how litter amount and texture affected seedling emergence and growth. Leaf litter was collected from an oakdominated hardwood stand and oven-dried at 70 8C for 4 days. Seeds were collected in October 2001, air dried, and separated from the fleshy fruit. To reduce the proportion of non-viable seeds, they were placed in water and those that floated were discarded. Remaining seeds were sterilized in a 10% bleach solution, rinsed and stratified in moist, sterilized sand for 40 days at 4 8C. The experiment used a two-way design with six litter amounts and two litter textures in four replications for a total of 48 pots. We planted 20 pre-treated seeds per pot approximately 5 mm deep in potting soil and covered with either fragmented (run through 6 mm mesh) or intact litter. The seeds were placed in a 20 cm2 circle within a 9 cm 9 cm pot. Pots were grouped into four blocks along a north–south axis in the same greenhouse used for the seed bank study. Litter amounts corresponding to 0, 1, 2, 4, 8 and 16 Mg ha1 were chosen to span the range of litterlayer depths that occur naturally in temperate deciduous forests (Sydes and Grime, 1981b; Kostel-Hughes et al., 1998b). The ‘‘no-litter’’ treatment represented complete displacement of the litter layer. The 16 Mg ha1 treatment provided litter conditions in excess of the natural range to increase the likelihood of encompassing the threshold at which an effect would be observed. Litter treatments were assigned randomly to pots in each block. Pots were kept well watered. Pins were placed next to each seedling as it emerged so that the timing and location of emergence (through or around litter) could be monitored. On day 56 after planting, seedlings were counted and five seedlings per pot with first true leaves >5 mm in length were randomly selected for harvest. We used the 5 mm length of true leaves as the criterion for harvest because at that point a seedling’s initial energy reserves appeared to be depleted. Each seedling was
partitioned into hypocotyl, radicle, and cotyledon components. Cotyledon area was measured using a computer scanner and Adobe Photoshop. Samples were oven-dried at 70 8C for 4 days and weighed. Statistical analysis was performed with the GLM procedure in SYSTAT 10.2 (SYSTAT Software Inc., Richmond, CA). The proportion of seedlings emerging was arcsine-square root transformed. Other variables were examined for homogeneity of variance graphically, and no further transformations were needed. The full experiment was analyzed first using the ANOVA model terms (and degrees of freedom): litter texture (intact versus fragmented) (1), litter amount (5), block (3), litter texture litter amount (5), and litter texture litter amount block (error) (33). One pot of the 16 Mg ha1 intact litter treatment had zero emergence, so it is missing from the analyses of seedling dimensions (hence the error term had 32 degrees of freedom). If no terms were significant at the P < 0:05 level, then no further analysis was performed. If the litter texture amount interaction was significant at the P < 0:10 level, the litter textures were analyzed again separately as a randomized block design with the following terms (and degrees of freedom): litter amount (5), block (3), litter amount block (error) (15). We used Fisher’s protected least significant difference test to determine if means of litter amounts greater than zero were different from those of the zero litter amount (within each litter texture if analyzed separately). We did not adjust the experiment-wise significance level because we were not testing post-hoc all pairs of means for differences.
3. Results 3.1. Seedling recruitment from seed rain versus seed bank Seedling recruitment from the seed bank contributed relatively little to establishment of C. orbiculatus in this forest. Under the 15 seed exclosures in the field only five seedlings germinated from the seed bank during the summer of 2001, which corresponds to a density of 0.9 m2. In the eight exclosures that remained intact until June 2002, no additional C. orbiculatus seedlings recruited. No C. orbiculatus seedlings emerged during the greenhouse tests of soil
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Fig. 1. Relationship between seed rain (m2) in 2000 and C. orbiculatus seedlings (m2) that emerged during the spring and summer 2001. Each point represents seedling emergence and seed trap data from one of the 15 sampling locations in a forest understory. Plotted line shows the geometric mean regression (slope ¼ 0:61, 95% CI ¼ 0:16, Y intercept not different from 0, r2 ¼ 0:82).
cores collected in the early fall of 2000, indicating that either there were no viable seeds or that conditions were not suitable for germination. Based on the high germination success of C. orbiculatus seeds in Experiment 2, we believe that conditions were conducive to germination. The soil cores did contain root fragments of C. orbiculatus that sprouted, but their lack of cotyledons enabled them to be distinguished from seedlings. In contrast to the seed exclosures, in the frames where seed rain was allowed and mammals excluded seedling recruitment ranged from 11 to 532 seedlings m2, with a mean of 107 m2 (Fig. 1). Seed rain ranged from 14 to 826 seeds m2 (Fig. 1), with a mean of 168 seeds m2. The close association between seed rain and seedling density (Fig. 1) means that spatial variability in seed input regulates seedling distribution. The regression intercept did not differ from zero (P ¼ 0:478), and the slope (0:61 0:16, 95% CI) was not distinguishable from the viability of collected seeds (0:66 0:08). This result supports the conclusion that little seedling recruitment derived from the seed bank. In addition, no seedlings emerged during greenhouse test of soil cores collected in the early fall of 2001, indicating that seeds that failed to germinate in the spring or summer of 2001 did not remain viable in the seed bank.
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Fig. 2. Emergence (%) of C. orbiculatus seedlings through intact (*) and fragmented (~) litter. Filled symbols indicate a significant difference from the value in the no-litter treatment for each litter type.
Fig. 3. Cotyledon area (a), hypocotyl length (b) and radicle length (c) of C. orbiculatus seedlings following emergence through intact (*) and fragmented (~) litter. Filled symbols indicate a significant difference from the value in the no-litter treatment for each litter type.
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Survival of seedlings in the frames ranged from 0 to 88%, with a mean of 17% (13 seedlings m2). Because the wire mesh on the frames prevented small mammal predation, and numerous wilted seedlings were observed, water stress or pathogens may have caused seedling mortality.
The effect of litter amount interacted with litter texture: seedling emergence decreased as intact litter increased, but significant differences were only detected between the no-litter and 16 Mg ha1 litter treatments (Fig. 2). Seedling emergence was not affected by fragmented litter (Fig. 2). Of the seedlings that emerged, a majority in the 4, 8 and 16 Mg ha1
intact litter treatments grew horizontally to emerge around the litter mass at the edge of the pot. This observation highlights the importance of hypocotyl elongation to seedling emergence in the forest floor. Litter texture and amount affected the size of seedling parts (Fig. 3a–c). Cotyledon area was decreased by intact versus fragmented litter, and amounts 4 Mg ha1 (Fig. 3a). Hypocotyl length increased with litter amount 2 Mg ha1 in the intact treatment but also with 4 Mg ha1 in the fragmented treatment (Fig. 3b). Radicle length decreased significantly only at 16 Mg ha1 in the intact treatment (Fig. 3c). The pattern of hypocotyl length increasing in response to the barrier of intact hardwood litter suggests that this increase was at the expense of the development of photosynthetic tissue or root tissue.
Fig. 4. Cotyledon mass (a), hypocotyl mass (b) and radicle mass (c) of C. orbiculatus seedlings following emergence through intact (*) and fragmented (~) litter. Filled symbol indicates a significant difference from the value in the no-litter treatment for each litter type.
Fig. 5. Ratio of cotyledon mass (a), hypocotyl mass (b) and radicle mass (c) to total seedling mass of C. orbiculatus seedlings following emergence through intact (*) and fragmented (~) litter. Filled symbols indicate a significant difference from the value in the no-litter treatment for each litter type.
3.2. Effects of litter amount and texture on seedling emergence and allocation
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The mass of cotyledons was not significantly altered by litter treatments, although it tended to decrease in intact litter and as litter mass increased (Fig. 4a). Hypocotyl mass increased in all intact litter treatments relative to 0 Mg ha1, but not in the fragmented litter (Fig. 4b). Radicle mass was lower under intact litter than fragmented litter, but decreased significantly from 0 Mg ha1only at 16 Mg ha1 (Fig. 4c). Although seedling total biomass was not affected by treatment, the variation in seedling mass can be accounted for by examining the relative allocation in terms of biomass ratios. The fraction of biomass in cotyledons decreased under intact litter compared to fragmented litter and at all quantities of litter (Fig. 5a). The biomass fraction of hypocotyl increased in intact relative to fragmented litter and was greater at 4 Mg ha1 and above in intact and in 2, 4 and 16 Mg ha1 of fragmented litter (Fig. 5b). Radicle mass ratio was lower in intact than fragmented litter, but significantly decreased only at 16 Mg ha1 (Fig. 5c). Allocation to hypocotyl growth in C. orbiculatus seedlings was plastic and was an important factor leading to seedling emergence from intact hardwood litter at quantities typical of the forest floor.
seeds in the traps, although both were observed; defleshed seeds that have passed through birds may have greater germination than those remaining in the fruits (Greenberg et al., 2001). Seed input and seedling emergence in the field were highly patchy, but relatively high densities of seedlings emerged when mammals were excluded (107 seedlings m2). Much higher densities are possible: C. orbiculatus fruits have been observed in small quadrats at densities above 400 fruits m2, which corresponded to seed densities of greater than 1600 m2 (Greenberg et al., 2001). Although we did not measure seedling density outside our exclosures, it appeared to be much lower, suggesting that animal predation is an important limit to the survival of C. orbiculatus seedlings. This suggestion is supported by high rates of mammal herbivory observed in another nearby field study (Ellsworth et al., in press). Because small mammal predation on seeds and seedlings is known to have a large effect on vegetation (Gill and Marks, 1991; Ostfeld et al., 1997), its role in controlling invasive plant establishment deserves further study.
4. Discussion
Our greenhouse study showed that the coarse texture of oak leaf litter was a barrier to C. orbiculatus seedlings because of its physical obstruction to emergence. Fragmented litter, which was similar chemically and completely shaded the soil surface, had no effect on emergence and much less on growth. However, a majority of seedlings were able to emerge from all but the highest amounts of intact litter, partly by increased allocation to hypocotyl elongation and biomass growth. We observed in the intact litter treatment that many but not all of the seedlings emerging at 4 Mg ha1, and all of the seedlings emerging at 8 and 16 Mg ha1, grew around the litter mass as far as the pot edge. The ability of hypocotyls to grow as long as 9 cm indicates that it is likely that C. orbiculatus seedlings could find a gap in the leaf litter in all but the densest forest floors. Forest floor mass in temperate deciduous forests during the summer is of the order of 6 Mg ha1 (Sydes and Grime, 1981b; Peterson and Facelli, 1992; Kostel-Hughes et al., 1998b) with leaf litterfall in autumn adding approximately 3 Mg ha1. Because a majority of C. orbiculatus seeds
4.1. Seedling recruitment Our results show that C. orbiculatus seedlings originate primarily from the current year’s seed input and that recruitment from the seed bank is minimal. Our conclusion is supported by the strong spatial association between seed input and seedling density and the low number of seedlings sprouting when seed rain was excluded. Other supporting evidence includes the lack of seedlings germinating from soil cores taken before and 1 year after the year 2000 seed crop, the relatively high germination rates of seeds in the lab (66%) and the similarity of seedling emergence as a fraction of seed input (61%) to viability estimates. The relatively low degree of seed bank persistence is most likely due to the high germination rate during the first summer. Germination rates in this experiment were comparable to those observed in other studies (Patterson, 1974; Dreyer et al., 1987; Greenberg et al., 2001). We did not distinguish fleshed from defleshed
4.2. Seeding emergence, growth, and allocation as affected by litter depth and texture
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are dispersed after litter fall (Greenberg et al., 2001), most seeds would become trapped in the less hospitable upper strata of the litter layer. Emergence success of many species are reduced when seeds are above or suspended in the litter layer (Fowler, 1986; Hamrick and Lee, 1987; Molofsky and Augspurger, 1992; Peterson and Facelli, 1992). In addition to the physical impediment of litter on radicle growth (Facelli and Pickett, 1991a), solar radiation can create extremely hot and dry conditions in the upper strata of the litter layer (Smith et al., 1997, p. 170). The effect of a litter layer between a germinating seed and the mineral soil was not addressed in this study, but would seem to increase the likelihood of mortality by drought or other stresses. The results of the fragmented litter treatment suggest that naturally fine-textured litter, such as conifer litter, may be more prone to invasion by C. orbiculatus. A forest floor under Eastern hemlock (Tsuga canadensis) of 23 Mg ha1 did not impede the emergence of Rhus typhina (Peterson and Facelli, 1992), which has seeds that are similar in size to C. orbiculatus. Biochemistry of litter from various species may also affect germination and growth, but was not addressed in our study. We did observe that closely clustered seedlings of C. orbiculatus apparently pushed together to raise the litter mass in fragmented and intact treatments. Such synchronous germination and growth was unforeseen but may be common in natural conditions. Each C. orbiculatus fruit contains four or five seeds (Patterson, 1974; Greenberg et al., 2001) and the clumped distribution of seed rain observed in our field study implies high localized seedling densities. The ability of C. orbiculatus seedlings to increase allocation to the hypocotyl at the expense of the cotyledons, thereby resulting in emergence from beneath dense forest floor agrees with the pattern shown by R. typhina (Peterson and Facelli, 1992). However, there may be costs to this shift in allocation, such as reduced initial photosynthetic area (Kitajima, 1994) and possibly greater susceptibility to physical damage (Aide, 1987; Clark and Clark, 1989; McCarthy and Facelli, 1990). In natural conditions where plants compete with neighboring vegetation, initial size differences will be compounded over time and can be a factor in the subsequent species composition of the local plant community (Ross and Harper, 1972; Uhl et al., 1988; Wilson, 1988).
4.3. Synthesis: management implications of C. orbiculatus establishment processes Native forest communities in the eastern United States are threatened by the spread of C. orbiculatus. Once established, C. orbiculatus vines can quickly overtop native vegetation on roadsides and in forest gaps and the species is recognized as a pest plant by land managers (Patterson, 1974; Dreyer et al., 1987; McNab and Meeker, 1987). Woody vines are well known to damage trees by above- and below-ground competition, girdling, physically linking and deforming stems, and suppressing regeneration (Schnitzer and Bongers, 2002). Our conclusions on the controls of C. orbiculatus establishment have several implications for management. If established plants and nearby seed sources are killed before the fruits mature, future recruitment will be limited to newly dispersed seeds and an occasional seed bank emergent. However, if a natural or human disturbance occurs after seeds have dispersed, high density populations are likely to be recruited. Once established, C. orbiculatus plants are able to photosynthesize and survive at very low light, and respond with rapid growth to partial or full sunlight (Ellsworth et al., in press). Vines rapidly proliferate following the creation of gaps by natural disturbance (Horvitz et al., 1998) and logging (Gerwing and Uhl, 2002). Relatively undisturbed forests may contain advance regeneration of C. orbiculatus because its seedlings are extremely good at penetrating forest floor litter, through plasticity in allocation to hypocotyl growth and apparently through positive interaction of multiple seedlings pushing through litter. It is unlikely that absence of forest floor disturbance would be adequate to prevent establishment of C. orbiculatus, although the causes of seedling mortality (e.g. mammal predation, environmental stresses, pathogens, seed location within the litter strata) and their interaction with growth rates remain to be determined.
Acknowledgements This research was supported by the USDA NRI Competitive Research Grants Program (award number 00-35320-9089), the Cooperative State Research Extension, Education Service, USDA, Massachusetts
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Agricultural Experiment Station, under Project No. 635889, 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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Ricard, J.P., Messier, C., 1996. Abundance, growth and allometry of red raspberry (Rubus idaeus L.) along a natural light gradient in a northern hardwood forest. For. Ecol. Manage. 81, 153–160. Roberts, H.A., 1981. Seed banks in soils. Adv. Appl. Biol. 6, 1–55. Ross, M.A., Harper, J.L., 1972. Occupation of biological space during seedling establishment. J. Ecol. 60, 77–88. Sanford, N.L., Harrington, R.A., Fownes, J.H., 2003. Survival and growth of native and alien woody seedlings in open and understory environments. For. Ecol. Manage. 183, 377–385. Schnitzer, S.A., Bongers, F., 2002. The ecology of lianas and their role in forests. Trends Ecol. Evol. 17, 223–230. Silveri, A., Dunwiddie, P.W., Michaels, H.J., 2001. Logging and edaphic factors in the invasion of an Asian woody vine in a mesic North American forest. Biol. Invas. 3, 379–389. Simpson, R.L., Leck, M.A., Parker, V.T., 1989. Seed banks: general concepts and methodological issues. In: Leck, M.A., Parker, V.T., Simpson, R.L. (Eds.), Ecology of Soil Seed Banks. Academic Press, New York, pp. 123–147. Smith, D.M., Larson, B.C., Kelty, M.J., Ashton, P.M.S., 1997. The Practice of Silviculture, 9th ed. Wiley, New York, p. 537. Sydes, C., Grime, J.P., 1981a. Effects of tree leaf litter on herbaceous vegetation in deciduous woodland. II. An experimental investigation. J. Ecol. 69, 248–262. Sydes, C., Grime, J.P., 1981b. Effects of tree leaf litter on herbaceous vegetation in deciduous woodland. I. Field investigations. J. Ecol. 69, 237–248.
The Nature Conservancy Connecticut Chapter in cooperation with The Natural Diversity Data Base of the Connecticut Department of Environmental Protection, 2002. Asiatic Bittersweet. http://www.hort.uconn.edu./ctpwg/art_pubs/TNC/html/nat_ orbitter.html. Thompson, K., 1987. Seeds and seed banks. New Phytol. 106 (Suppl.), 23–34. Thompson, K., Grime, J.P., 1979. Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. J. Ecol. 67, 893–921. Uhl, C.K., Clark, K., Dezzo, N., Maquirino, P., 1988. Vegetation dynamics in Amazonian tree fall gaps. Ecology 69, 751–763. Webb, S.A., Kaunzinger, C.K., 1993. Biological invasion of the Drew University (New Jersey) Forest Preserve by Norway Maple (Acer platanoides L.) Bull. Torrey Bot. Club 120, 343– 349. Wendel, G.W., 1990. Pin cherry: Prunus pensylvanica L.f. In: Silvics of North America. 2. Hardwoods. US Department of Agriculture Agricultural Handbook No. 654. US Government Printing Office, Washington, DC, p. 877. Wilson, J.B., 1988. The effect of initial advantage on the course of plant competition. Oikos 51, 19–24. Woods, K.D., 1993. Effects of invasion by Lonicera tartarica L. on herbs and tree seedlings in four New England Forests. Am. Midl. Nat. 130, 62–74.
Seedling emergence, growth, and allocation of Oriental bittersweet: effects of seed input, seed bank, and forest floor litter Joshua W. Ellsworth, Robin A. Harrington*, James H. Fownes Department of Natural Resources Conservation, University of Massachusetts at Amherst, Amherst, MA 01003, USA Received 28 July 2003; received in revised form 24 September 2003; accepted 12 October 2003
Abstract The establishment of invasive plant populations is controlled by seed input, survival in the soil seed bank, and effects of soil surface disturbance on emergence, growth, and survival. We studied the invasive vine Celastrus orbiculatus Thunb. (Oriental bittersweet) to determine if seedlings in forest understory germinate from the seed bank or from seed rain. We also conducted a greenhouse experiment to investigate the role of leaf litter mass and physical texture on seedling survival, growth, and allocation. In the understory of an invaded mixed hardwood forest, we measured seed input, seedling emergence with seed rain, and seedling emergence without seed rain. Mean seed rain was 168 seeds m2: mean seedling emergence was 107 m2, and there was a strong correlation between seed rain and seedling emergence. The ratio of seedlings to seed input (0.61) was close to the seed viability (0.66) leaving very few seeds to enter the seed bank. Seed bank germination under field conditions was low (1 seedling m2). Soil cores were incubated in a greenhouse to determine seed bank viability, and germination from these soil cores did not occur. To determine how litter affects seedling establishment and growth, we measured seedling emergence and biomass allocation in a greenhouse experiment. Seeds were placed below intact and fragmented deciduous leaf litter in amounts ranging from zero to the equivalent of 16 Mg ha1. Seedling emergence was not affected by fragmented litter, but decreased to <20% as intact litter increased to 16 Mg ha1. Increasing litter resulted in greater allocation to hypocotyl and less to cotyledon and radicle, and this effect was greater in intact litter. C. orbiculatus seedlings achieve emergence through forest floor litter through plasticity in allocation to hypocotyl growth. The low survival of C. orbiculatus in the seed bank suggests that eradication of seedling advance regeneration and adult plants prior to seed rain may be an effective control strategy. However, the intact forest floor litter of an undisturbed forest will not prevent seedling establishment. # 2003 Elsevier B.V. All rights reserved. Keywords: Celastrus orbiculatus; Forest understory; Invasive species; Seed rain
1. Introduction Plant invasions are often associated with disturbances (e.g. Mazia et al., 2001; McNab and Loftis, *
Corresponding author. Tel.: þ1-413-577-0204; fax: þ1-413-545-4358. E-mail address: [email protected] (R.A. Harrington).
2002), but several non-native woody species have successfully invaded relatively undisturbed forests (Luken, 1988; Harrington et al., 1989; Webb and Kaunzinger, 1993; Woods, 1993; Cassidy et al., in press). Although shade and nutrient availability may limit the growth of invaders once they are established (Cassidy et al., in press; Sanford et al., 2003; Ellsworth et al., in press), the fates of seeds and seedlings
0378-1127/$ – see front matter # 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2003.10.015
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determine establishment in the understory and therefore have important implications for forest management. If enough seeds germinate and survive, then populations can establish that may grow slowly but respond rapidly to release by canopy opening (Greenberg et al., 2001). Conversely, if seeds remain viable in the soil, they can accumulate into a seed bank that is capable of response to soil disturbance (Paynter et al., 1998). In this case, survival in the soil seed bank and how soil surface disturbance affects emergence, growth, and survival are key controls on the establishment of invader populations. The purpose of this research was to determine whether Celastrus orbiculatus Thunb. (Oriental bittersweet), an invasive woody vine from eastern Asia, forms a seed bank and how forest floor disturbance affects its germination, growth and seedling survival. Seeds of C. orbiculatus mature in autumn and are dispersed by birds and mammals throughout the fall, winter and early spring (Patterson, 1974; Greenberg et al., 2001; Silveri et al., 2001). It is not clear whether seeds of C. orbiculatus can remain dormant in the seed bank. Seed bank longevity varies widely between species (Roberts, 1981; Thompson, 1987; Simpson et al., 1989), ranging from transient seed banks, where seeds persist only through the summer, to persistent seed banks, where viable seeds can last for decades (Thompson and Grime, 1979; Baskin and Baskin, 1989). If a species’ seeds persist in the seed bank, delayed germination may be triggered by natural or human-caused disturbances, such as logging or road building, that turn the soil or increase light levels at the forest floor (Livingston and Leck, 1968; Thompson, 1987; Baskin and Baskin, 1989; Ricard and Messier, 1996). Furthermore, control programs timed to kill seed-bearing plants prior to fruit maturation may stop the dispersal of a new seed crop, but do not ensure that dormant seeds present on site would not germinate in the future. Although some land managers report that C. orbiculatus seeds persist in the seed bank (The Nature Conservancy Connecticut Chapter, 2002), a 2-year experiment in a greenhouse did not detect germination after 1 year (Kostel-Hughes et al., 1998a). Many seed bank species have small seeds, often less than 2 or 3 mg (Pickett and McDonnell, 1989), which may decrease detection by seed predators (Thompson, 1987). By contrast, C. orbiculatus seeds weigh
10–12 mg (Patterson, 1974; our observations). Larger-seeded species that persist in the seed bank, such as Prunus pensylvanica (pin cherry), have thick seed coats (Wendel, 1990). Unlike P. pensylvanica, however, C. orbiculatus does not require mechanical or chemical scarification prior to germination (Patterson, 1974; Greenberg et al., 2001; our observations), suggesting that its seed coat is not sufficiently thick to protect it through multiple years of burial in the soil. Therefore, we hypothesized that C. orbiculatus would not persist in the seed bank, and that the previous year’s seed rain is the main source of seedling recruits. Forest floor litter decreases germination and seedling emergence through shading, biochemical effects, and physical obstruction to the emergence of a seed’s cotyledons and radicle (Sydes and Grime, 1981a; Facelli and Pickett, 1991a; Guzman-Grajales and Walker, 1991; Molofsky and Augspurger, 1992). Physical obstruction may either prevent seedling emergence or force seedlings to allocate more stored energy to hypocotyl growth in order to penetrate the litter layer, leaving less energy for allocation to the radicle and cotyledons. Such changes in allocation result in spindly, less sturdy seedlings with reduced ability to capture light, water, and nutrients (Facelli and Pickett, 1991a,b; Peterson and Facelli, 1992). Litter texture may also influence establishment, with coarse litter being more difficult to penetrate than fine litter (Peterson and Facelli, 1992). Many plant species require disturbances of the soil surface or organic litter layer in order to become established, in part because of the barrier posed by leaf litter (Keever, 1973; Marks, 1983; Facelli and Pickett, 1991a). Surveys of forest tracts show that C. orbiculatus is more common along logging roads (Silveri et al., 2001) and in areas that experience soil and litter disturbance from logging, windthrow, and foraging wildlife (McNab and Loftis, 2002). Litterlayer mass also varies naturally locally (Sydes and Grime, 1981b) and over time due to seasonal fluxes in decomposition rates and input (Facelli and Pickett, 1991a). Seasonal fluctuations in litter-layer mass are especially pertinent to C. orbiculatus because fruits mature in late September and can remain on the vine through the winter. Thus, viable seeds are dispersed into a wide range of natural litter conditions. We hypothesized that the emergence success of C. orbiculatus would decrease with increasing litter mass and
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that successful establishment of C. orbiculatus seeds would be greater when seeds were placed below fragmented litter rather than equal amounts of intact litter. We also hypothesized that increasing litter mass and coarseness would cause C. orbiculatus seedlings to allocate more to hypocotyls and therefore less to cotyledons and radicles.
the spring and summer of 2001 as a measure of germination from seeds that had been dormant for 1 year. One year later, in 2002, eight exclosures were still intact and were examined in mid-June for any further seedling recruitment. Seedlings were distinguished from root sprouts by the presence of cotyledons.
2. Methods
2.3. Experiment I: seedling recruitment from seed rain
2.1. Site description We conducted both field and greenhouse experiments to investigate factors that influence C. orbiculatus establishment. The source population was a dense population of fruit-producing C. orbiculatus vines in the canopy of a young, mixed-deciduous stand in the Sylvan Woods of the Waugh Arboretum, University of Massachusetts, Amherst. Dominant canopy-tree species included northern red oak (Quercus rubra), hickory (Carya spp.), and red maple (Acer rubrum), and the shrub layer was dominated by honeysuckle (Lonicera spp.).
Seed rain from the 2000 seed crop was estimated from seeds trapped by the exclosures in subplot 1 (Section 2.2). We collected seeds from the traps in May 2001. In subplot 2, a frame covered only with 6 mm wide mesh allowed C. orbiculatus seeds from seed rain to enter the soil, but protected them from herbivory. Seedlings were counted during the summer of 2001. The ratio of seedlings recruited to seed input was estimated from the slope of the geometric mean regression (GMR) between numbers of seedlings and number of seeds in paired subplots (Krebs, 1999, p. 559). Survival of seedlings under the frames was measured through August 2001.
2.2. Experiment I: seedling recruitment from seed bank
2.4. Experiment I: viability of seed rain and seed bank
To assess the potential importance of a seed bank to seedling recruitment, we experimentally compared seedling recruitment in 2001 with and without seed rain from the 2000 growing season. In the fall of 2000 (before seed rain), we selected 15 sampling locations beneath the vine canopy. At each we laid out four 61 cm 61 cm (0.37 m2) subplots. The subplots at each site were used to measure three variables: (1) seed bank germination in field conditions, (2) seed bank germination in greenhouse conditions (viability of the seed bank), and (3) the proportion of seed rain that germinated the first year after dispersal. Seedling recruitment from the seed bank was estimated from subplot 1 using exclosures that prevented the 2000 seed crop from reaching the soil. Exclosures were wooden frames covered with 2 mm screen to catch seed. A second frame with 6 mm wire mesh was placed on top of the fine screen to protect fruits and seeds from animal consumption. Seedlings recruiting under the mesh were tagged and counted throughout
We assessed viability of seeds in seed rain by collecting C. orbiculatus fruits from vines in April 2000, air-drying them for 30 days and removing the seeds. One hundred and forty-three seeds were kept moist for 41 days at 18 8C and checked for germination success. The 95% confidence limits for the proportion of viable seeds was calculated using a binomial distribution (Krebs, 1999, p. 270). Seed bank viability was tested in greenhouse conditions. Five subsamples of the A soil horizon were collected in mid-October 2000 from the subplot 3 at each location using a 7 cm diameter bulb planter. The five subsamples were pooled and stored in plastic bags at 4 8C. for 80 days. Each sample was then spread out to a depth of less than 1.75 cm on top of potting soil in flats and placed in greenhouse with ambient light measuring 40% of full sun. Flats were well watered. The emergence of C. orbiculatus seedlings was monitored for 60 days. We also collected soil cores from the subplot 4 in early fall 2001 to assess if seeds from
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the 2000 seed rain remained viable in the seed bank. The collection and germination methods followed those in the previous greenhouse study. 2.5. Experiment II: response to litter amount and texture We conducted a greenhouse study to examine how litter amount and texture affected seedling emergence and growth. Leaf litter was collected from an oakdominated hardwood stand and oven-dried at 70 8C for 4 days. Seeds were collected in October 2001, air dried, and separated from the fleshy fruit. To reduce the proportion of non-viable seeds, they were placed in water and those that floated were discarded. Remaining seeds were sterilized in a 10% bleach solution, rinsed and stratified in moist, sterilized sand for 40 days at 4 8C. The experiment used a two-way design with six litter amounts and two litter textures in four replications for a total of 48 pots. We planted 20 pre-treated seeds per pot approximately 5 mm deep in potting soil and covered with either fragmented (run through 6 mm mesh) or intact litter. The seeds were placed in a 20 cm2 circle within a 9 cm 9 cm pot. Pots were grouped into four blocks along a north–south axis in the same greenhouse used for the seed bank study. Litter amounts corresponding to 0, 1, 2, 4, 8 and 16 Mg ha1 were chosen to span the range of litterlayer depths that occur naturally in temperate deciduous forests (Sydes and Grime, 1981b; Kostel-Hughes et al., 1998b). The ‘‘no-litter’’ treatment represented complete displacement of the litter layer. The 16 Mg ha1 treatment provided litter conditions in excess of the natural range to increase the likelihood of encompassing the threshold at which an effect would be observed. Litter treatments were assigned randomly to pots in each block. Pots were kept well watered. Pins were placed next to each seedling as it emerged so that the timing and location of emergence (through or around litter) could be monitored. On day 56 after planting, seedlings were counted and five seedlings per pot with first true leaves >5 mm in length were randomly selected for harvest. We used the 5 mm length of true leaves as the criterion for harvest because at that point a seedling’s initial energy reserves appeared to be depleted. Each seedling was
partitioned into hypocotyl, radicle, and cotyledon components. Cotyledon area was measured using a computer scanner and Adobe Photoshop. Samples were oven-dried at 70 8C for 4 days and weighed. Statistical analysis was performed with the GLM procedure in SYSTAT 10.2 (SYSTAT Software Inc., Richmond, CA). The proportion of seedlings emerging was arcsine-square root transformed. Other variables were examined for homogeneity of variance graphically, and no further transformations were needed. The full experiment was analyzed first using the ANOVA model terms (and degrees of freedom): litter texture (intact versus fragmented) (1), litter amount (5), block (3), litter texture litter amount (5), and litter texture litter amount block (error) (33). One pot of the 16 Mg ha1 intact litter treatment had zero emergence, so it is missing from the analyses of seedling dimensions (hence the error term had 32 degrees of freedom). If no terms were significant at the P < 0:05 level, then no further analysis was performed. If the litter texture amount interaction was significant at the P < 0:10 level, the litter textures were analyzed again separately as a randomized block design with the following terms (and degrees of freedom): litter amount (5), block (3), litter amount block (error) (15). We used Fisher’s protected least significant difference test to determine if means of litter amounts greater than zero were different from those of the zero litter amount (within each litter texture if analyzed separately). We did not adjust the experiment-wise significance level because we were not testing post-hoc all pairs of means for differences.
3. Results 3.1. Seedling recruitment from seed rain versus seed bank Seedling recruitment from the seed bank contributed relatively little to establishment of C. orbiculatus in this forest. Under the 15 seed exclosures in the field only five seedlings germinated from the seed bank during the summer of 2001, which corresponds to a density of 0.9 m2. In the eight exclosures that remained intact until June 2002, no additional C. orbiculatus seedlings recruited. No C. orbiculatus seedlings emerged during the greenhouse tests of soil
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Fig. 1. Relationship between seed rain (m2) in 2000 and C. orbiculatus seedlings (m2) that emerged during the spring and summer 2001. Each point represents seedling emergence and seed trap data from one of the 15 sampling locations in a forest understory. Plotted line shows the geometric mean regression (slope ¼ 0:61, 95% CI ¼ 0:16, Y intercept not different from 0, r2 ¼ 0:82).
cores collected in the early fall of 2000, indicating that either there were no viable seeds or that conditions were not suitable for germination. Based on the high germination success of C. orbiculatus seeds in Experiment 2, we believe that conditions were conducive to germination. The soil cores did contain root fragments of C. orbiculatus that sprouted, but their lack of cotyledons enabled them to be distinguished from seedlings. In contrast to the seed exclosures, in the frames where seed rain was allowed and mammals excluded seedling recruitment ranged from 11 to 532 seedlings m2, with a mean of 107 m2 (Fig. 1). Seed rain ranged from 14 to 826 seeds m2 (Fig. 1), with a mean of 168 seeds m2. The close association between seed rain and seedling density (Fig. 1) means that spatial variability in seed input regulates seedling distribution. The regression intercept did not differ from zero (P ¼ 0:478), and the slope (0:61 0:16, 95% CI) was not distinguishable from the viability of collected seeds (0:66 0:08). This result supports the conclusion that little seedling recruitment derived from the seed bank. In addition, no seedlings emerged during greenhouse test of soil cores collected in the early fall of 2001, indicating that seeds that failed to germinate in the spring or summer of 2001 did not remain viable in the seed bank.
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Fig. 2. Emergence (%) of C. orbiculatus seedlings through intact (*) and fragmented (~) litter. Filled symbols indicate a significant difference from the value in the no-litter treatment for each litter type.
Fig. 3. Cotyledon area (a), hypocotyl length (b) and radicle length (c) of C. orbiculatus seedlings following emergence through intact (*) and fragmented (~) litter. Filled symbols indicate a significant difference from the value in the no-litter treatment for each litter type.
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Survival of seedlings in the frames ranged from 0 to 88%, with a mean of 17% (13 seedlings m2). Because the wire mesh on the frames prevented small mammal predation, and numerous wilted seedlings were observed, water stress or pathogens may have caused seedling mortality.
The effect of litter amount interacted with litter texture: seedling emergence decreased as intact litter increased, but significant differences were only detected between the no-litter and 16 Mg ha1 litter treatments (Fig. 2). Seedling emergence was not affected by fragmented litter (Fig. 2). Of the seedlings that emerged, a majority in the 4, 8 and 16 Mg ha1
intact litter treatments grew horizontally to emerge around the litter mass at the edge of the pot. This observation highlights the importance of hypocotyl elongation to seedling emergence in the forest floor. Litter texture and amount affected the size of seedling parts (Fig. 3a–c). Cotyledon area was decreased by intact versus fragmented litter, and amounts 4 Mg ha1 (Fig. 3a). Hypocotyl length increased with litter amount 2 Mg ha1 in the intact treatment but also with 4 Mg ha1 in the fragmented treatment (Fig. 3b). Radicle length decreased significantly only at 16 Mg ha1 in the intact treatment (Fig. 3c). The pattern of hypocotyl length increasing in response to the barrier of intact hardwood litter suggests that this increase was at the expense of the development of photosynthetic tissue or root tissue.
Fig. 4. Cotyledon mass (a), hypocotyl mass (b) and radicle mass (c) of C. orbiculatus seedlings following emergence through intact (*) and fragmented (~) litter. Filled symbol indicates a significant difference from the value in the no-litter treatment for each litter type.
Fig. 5. Ratio of cotyledon mass (a), hypocotyl mass (b) and radicle mass (c) to total seedling mass of C. orbiculatus seedlings following emergence through intact (*) and fragmented (~) litter. Filled symbols indicate a significant difference from the value in the no-litter treatment for each litter type.
3.2. Effects of litter amount and texture on seedling emergence and allocation
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The mass of cotyledons was not significantly altered by litter treatments, although it tended to decrease in intact litter and as litter mass increased (Fig. 4a). Hypocotyl mass increased in all intact litter treatments relative to 0 Mg ha1, but not in the fragmented litter (Fig. 4b). Radicle mass was lower under intact litter than fragmented litter, but decreased significantly from 0 Mg ha1only at 16 Mg ha1 (Fig. 4c). Although seedling total biomass was not affected by treatment, the variation in seedling mass can be accounted for by examining the relative allocation in terms of biomass ratios. The fraction of biomass in cotyledons decreased under intact litter compared to fragmented litter and at all quantities of litter (Fig. 5a). The biomass fraction of hypocotyl increased in intact relative to fragmented litter and was greater at 4 Mg ha1 and above in intact and in 2, 4 and 16 Mg ha1 of fragmented litter (Fig. 5b). Radicle mass ratio was lower in intact than fragmented litter, but significantly decreased only at 16 Mg ha1 (Fig. 5c). Allocation to hypocotyl growth in C. orbiculatus seedlings was plastic and was an important factor leading to seedling emergence from intact hardwood litter at quantities typical of the forest floor.
seeds in the traps, although both were observed; defleshed seeds that have passed through birds may have greater germination than those remaining in the fruits (Greenberg et al., 2001). Seed input and seedling emergence in the field were highly patchy, but relatively high densities of seedlings emerged when mammals were excluded (107 seedlings m2). Much higher densities are possible: C. orbiculatus fruits have been observed in small quadrats at densities above 400 fruits m2, which corresponded to seed densities of greater than 1600 m2 (Greenberg et al., 2001). Although we did not measure seedling density outside our exclosures, it appeared to be much lower, suggesting that animal predation is an important limit to the survival of C. orbiculatus seedlings. This suggestion is supported by high rates of mammal herbivory observed in another nearby field study (Ellsworth et al., in press). Because small mammal predation on seeds and seedlings is known to have a large effect on vegetation (Gill and Marks, 1991; Ostfeld et al., 1997), its role in controlling invasive plant establishment deserves further study.
4. Discussion
Our greenhouse study showed that the coarse texture of oak leaf litter was a barrier to C. orbiculatus seedlings because of its physical obstruction to emergence. Fragmented litter, which was similar chemically and completely shaded the soil surface, had no effect on emergence and much less on growth. However, a majority of seedlings were able to emerge from all but the highest amounts of intact litter, partly by increased allocation to hypocotyl elongation and biomass growth. We observed in the intact litter treatment that many but not all of the seedlings emerging at 4 Mg ha1, and all of the seedlings emerging at 8 and 16 Mg ha1, grew around the litter mass as far as the pot edge. The ability of hypocotyls to grow as long as 9 cm indicates that it is likely that C. orbiculatus seedlings could find a gap in the leaf litter in all but the densest forest floors. Forest floor mass in temperate deciduous forests during the summer is of the order of 6 Mg ha1 (Sydes and Grime, 1981b; Peterson and Facelli, 1992; Kostel-Hughes et al., 1998b) with leaf litterfall in autumn adding approximately 3 Mg ha1. Because a majority of C. orbiculatus seeds
4.1. Seedling recruitment Our results show that C. orbiculatus seedlings originate primarily from the current year’s seed input and that recruitment from the seed bank is minimal. Our conclusion is supported by the strong spatial association between seed input and seedling density and the low number of seedlings sprouting when seed rain was excluded. Other supporting evidence includes the lack of seedlings germinating from soil cores taken before and 1 year after the year 2000 seed crop, the relatively high germination rates of seeds in the lab (66%) and the similarity of seedling emergence as a fraction of seed input (61%) to viability estimates. The relatively low degree of seed bank persistence is most likely due to the high germination rate during the first summer. Germination rates in this experiment were comparable to those observed in other studies (Patterson, 1974; Dreyer et al., 1987; Greenberg et al., 2001). We did not distinguish fleshed from defleshed
4.2. Seeding emergence, growth, and allocation as affected by litter depth and texture
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are dispersed after litter fall (Greenberg et al., 2001), most seeds would become trapped in the less hospitable upper strata of the litter layer. Emergence success of many species are reduced when seeds are above or suspended in the litter layer (Fowler, 1986; Hamrick and Lee, 1987; Molofsky and Augspurger, 1992; Peterson and Facelli, 1992). In addition to the physical impediment of litter on radicle growth (Facelli and Pickett, 1991a), solar radiation can create extremely hot and dry conditions in the upper strata of the litter layer (Smith et al., 1997, p. 170). The effect of a litter layer between a germinating seed and the mineral soil was not addressed in this study, but would seem to increase the likelihood of mortality by drought or other stresses. The results of the fragmented litter treatment suggest that naturally fine-textured litter, such as conifer litter, may be more prone to invasion by C. orbiculatus. A forest floor under Eastern hemlock (Tsuga canadensis) of 23 Mg ha1 did not impede the emergence of Rhus typhina (Peterson and Facelli, 1992), which has seeds that are similar in size to C. orbiculatus. Biochemistry of litter from various species may also affect germination and growth, but was not addressed in our study. We did observe that closely clustered seedlings of C. orbiculatus apparently pushed together to raise the litter mass in fragmented and intact treatments. Such synchronous germination and growth was unforeseen but may be common in natural conditions. Each C. orbiculatus fruit contains four or five seeds (Patterson, 1974; Greenberg et al., 2001) and the clumped distribution of seed rain observed in our field study implies high localized seedling densities. The ability of C. orbiculatus seedlings to increase allocation to the hypocotyl at the expense of the cotyledons, thereby resulting in emergence from beneath dense forest floor agrees with the pattern shown by R. typhina (Peterson and Facelli, 1992). However, there may be costs to this shift in allocation, such as reduced initial photosynthetic area (Kitajima, 1994) and possibly greater susceptibility to physical damage (Aide, 1987; Clark and Clark, 1989; McCarthy and Facelli, 1990). In natural conditions where plants compete with neighboring vegetation, initial size differences will be compounded over time and can be a factor in the subsequent species composition of the local plant community (Ross and Harper, 1972; Uhl et al., 1988; Wilson, 1988).
4.3. Synthesis: management implications of C. orbiculatus establishment processes Native forest communities in the eastern United States are threatened by the spread of C. orbiculatus. Once established, C. orbiculatus vines can quickly overtop native vegetation on roadsides and in forest gaps and the species is recognized as a pest plant by land managers (Patterson, 1974; Dreyer et al., 1987; McNab and Meeker, 1987). Woody vines are well known to damage trees by above- and below-ground competition, girdling, physically linking and deforming stems, and suppressing regeneration (Schnitzer and Bongers, 2002). Our conclusions on the controls of C. orbiculatus establishment have several implications for management. If established plants and nearby seed sources are killed before the fruits mature, future recruitment will be limited to newly dispersed seeds and an occasional seed bank emergent. However, if a natural or human disturbance occurs after seeds have dispersed, high density populations are likely to be recruited. Once established, C. orbiculatus plants are able to photosynthesize and survive at very low light, and respond with rapid growth to partial or full sunlight (Ellsworth et al., in press). Vines rapidly proliferate following the creation of gaps by natural disturbance (Horvitz et al., 1998) and logging (Gerwing and Uhl, 2002). Relatively undisturbed forests may contain advance regeneration of C. orbiculatus because its seedlings are extremely good at penetrating forest floor litter, through plasticity in allocation to hypocotyl growth and apparently through positive interaction of multiple seedlings pushing through litter. It is unlikely that absence of forest floor disturbance would be adequate to prevent establishment of C. orbiculatus, although the causes of seedling mortality (e.g. mammal predation, environmental stresses, pathogens, seed location within the litter strata) and their interaction with growth rates remain to be determined.
Acknowledgements This research was supported by the USDA NRI Competitive Research Grants Program (award number 00-35320-9089), the Cooperative State Research Extension, Education Service, USDA, Massachusetts
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Agricultural Experiment Station, under Project No. 635889, 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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