Download Seedling emergence, growth, and allocation of Oriental bittersweet

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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J.W. Ellsworth et al. / Forest Ecology and Management 190 (2004) 255–264
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
J.W. Ellsworth et al. / Forest Ecology and Management 190 (2004) 255–264
257
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
J.W. Ellsworth et al. / Forest Ecology and Management 190 (2004) 255–264
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.
259
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
J.W. Ellsworth et al. / Forest Ecology and Management 190 (2004) 255–264
261
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
J.W. Ellsworth et al. / Forest Ecology and Management 190 (2004) 255–264
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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