Diversity and Distributions, (Diversity Distrib.) (2008) 14, 169–178
Blackwell Publishing Ltd
BIODIVERSITY
RESEARCH
Tolerance to herbivory, and not
resistance, may explain differential
success of invasive, naturalized, and
native North American temperate vines
Isabel W. Ashton*,† and Manuel T. Lerdau
Department of Ecology and Evolution,
State University of New York at Stony Brook,
Stony Brook, New York 11794, USA
*Correspondence: Isabel W. Ashton,
Department of Ecology and Evolution,
State University of New York at Stony Brook,
Stony Brook, New York 11794, USA.
E-mail: [email protected]
†Present address: Department of Ecology
and Evolutionary Biology, University of
California, Irvine, 321 Steinhaus Hall, Irvine,
CA 92697-2525, USA.
ABSTRACT
Numerous hypotheses suggest that natural enemies can influence the dynamics of
biological invasions. Here, we use a group of 12 related native, invasive, and naturalized
vines to test the relative importance of resistance and tolerance to herbivory in
promoting biological invasions. In a field experiment in Long Island, New York,
we excluded mammal and insect herbivores and examined plant growth and foliar
damage over two growing seasons. This novel approach allowed us to compare the
relative damage from mammal and insect herbivores and whether damage rates were
related to invasion. In a greenhouse experiment, we simulated herbivory through
clipping and measured growth response. After two seasons of excluding herbivores,
there was no difference in relative growth rates among invasive, naturalized, and
native woody vines, and all vines were susceptible to damage from mammal and insect
herbivores. Thus, differential attack by herbivores and plant resistance to herbivory
did not explain invasion success of these species. In the field, where damage rates
were high, none of the vines were able to fully compensate for damage from mammals. However, in the greenhouse, we found that invasive vines were more tolerant
of simulated herbivory than native and naturalized relatives. Our results indicate
that invasive vines are not escaping herbivory in the novel range, rather they are
persisting despite high rates of herbivore damage in the field. While most studies of
invasive plants and natural enemies have focused on resistance, this work suggests
that tolerance may also play a large role in facilitating invasions.
Keywords
Ampelopsis, biological invasions, Celastrus, Clematis, Lonicera, natural enemies.
Biological invasions are a major component of global change,
and numerous hypotheses have been developed to explore the
mechanisms responsible for invasion success. In particular, there
has been a widespread effort to explore how natural enemies
affect the invasion process (e.g. Elton, 1958; Blossey & Notzold,
1995; Maron & Vila, 2001; Keane & Crawley, 2002; Blumenthal,
2005, 2006). The manner and degree to which plants, whether
native or introduced, interact with the herbivore community
varies greatly, and there are generally considered to be two important components involved in plant response to herbivores:
resistance and tolerance (Marquis, 1992). Resistance refers to
any plant trait, such as plant secondary chemistry, that reduces
the preference or performance of herbivores, and tolerance refers
to the ability of a plant to maintain its reproductive fitness even
with tissue loss caused by herbivory (Rosenthal & Kotanen, 1994;
Strauss & Agrawal, 1999). Most studies of invasive plants and
natural enemies have focused on resistance (e.g. Agrawal et al.,
2005), but there has been a recent increase in the recognition that
tolerance may also play a role in facilitating successful invasions
(Rogers & Siemann, 2004; Murren et al., 2005; Stastny et al.,
2005).
Invasive species may persist because they possess traits that
make them more resistant to enemies than co-occurring native
species (e.g. Daehler & Strong, 1997; Leger & Forister, 2005).
More often, however, it is thought that invasive species experience a relaxation of enemy pressure in the novel environment
because of an absence of specialist herbivores, and thus selection
favours genotypes that allocate less to defence and more to
growth (Blossey & Notzold, 1995; Bossdorf et al., 2004; Maron
et al., 2004; Stastny et al., 2005). Whether an invader experiences
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd
DOI: 10.1111/j.1472-4642.2007.00425.x
www.blackwellpublishing.com/ddi
INTRODUCTION
169
I. W. Ashton and M. T. Lerdau
reduced herbivore pressure in the novel range due to escape or
resistance, this reduction should translate into low damage rates
in the field. Despite the general interest in natural enemies and
invasions, field studies examining damage to invasive species are
still relatively scarce, and the results vary considerably. Depending on the species and experiment, researchers have observed
that invasive species suffer lower, higher, or similar damage rates
compared to natives (Daehler, 2003; Levine et al., 2004; Carpenter
& Cappuccino, 2005; Parker et al., 2006). Damage rates may vary
depending on herbivore identity. While most studies have
focused on insect herbivores, the few that have used mammal
herbivores tend to find similar damage rates across invasive and
native plants (Schierenbeck et al., 1994; Parker et al., 2006). These
different outcomes may depend on whether the invasive is phylogenetically similar to native plants, causing it to be palatable to
native herbivores, or phylogenetically distant, thus attracting
fewer herbivores in its new range (Mitchell et al., 2006; Parker
et al., 2006). Furthermore, plant resistance can also vary in space
and time (Agrawal et al., 2005) due to interactions with the biotic
and abiotic environment (Mitchell et al., 2006), making results
from short-term experiments difficult to interpret.
An alternate possibility is that invasive plants tolerate herbivory more than native species (Schierenbeck et al., 1994; Rogers &
Siemann, 2003, 2004; Stastny et al., 2005). For plants, there are
numerous mechanisms involved in tolerance, including increasing photosynthetic rates after damage, increasing branching,
high relative growth rates, and shifting stores between aboveand below-ground pools (Marquis, 1992; Throop & Fay, 1999;
Tiffin, 2000). Compensatory growth and tolerance have been
implicated in the success of invasive plants (Kimball & Schiffman,
2003; Rogers & Siemann, 2003; Bossdorf et al., 2004; Rogers &
Siemann, 2004; Stastny et al., 2005). Most of these studies, however,
have focused on single invaders, and it is not known how common
high tolerance is among invasives.
As efforts move forward to develop a more comprehensive
understanding of biological invasions, one challenge is to discover
the general patterns (if any exist) that unite invasive taxa and distinguish them from natives and from other alien taxa that become
established but not invasive. By examining aliens that have
become established but are not invasive (hereafter, naturalized),
it becomes possible to determine whether traits shared by invasives are, in fact, linked to the success of the invasive taxon and
therefore absent in naturalized taxa (Mack, 1996; Rejmánek &
Richardson, 1996; Reichard & Hamilton, 1997; Muth & Pigliucci,
2006). Although the approach of contrasting invasive and naturalized species has been used recently for field and greenhouse
surveys (Smith & Knapp, 2001; Grotkopp et al., 2002; McDowell,
2002; Dark, 2004; Cappuccino & Arnason, 2006), few experimental studies with this approach have been carried out (but, see
Burns, 2004; Muth & Pigliucci, 2006 for notable exceptions).
Another challenge in developing a more comprehensive understanding of the plant traits associated with invasion lies in the
fact that plant taxa can show great variability in physiological and
ecological traits causing differences between invasive and naturalized or native plants to be confounded with phylogeny. One
powerful approach used to reduce the effects of phylogeny is to
compare native, invasive, and naturalized taxa within the same
genus or family (Mack, 1996; Agrawal & Kotanen, 2003). For
instance, this approach has been used to determine that invasive
plants when compared to naturalized plants are more likely to
possess secondary compounds that are not found in native
plants, suggesting that novel chemistry may add to herbivore
resistance and invasion success (Cappuccino & Arnason, 2006).
Woody vines can be aggressive invasive plants and are becoming increasingly abundant in temperate forests (Teramura et al.,
1991; Schierenbeck et al., 1994). As with many invasive species,
little is known about the factors limiting the distribution and
growth of invasive vines (Bell et al., 1988; Putz & Holbrook,
1991; Schnitzer & Bongers, 2002). Mammals often have strong
impacts on plant communities, but their impacts on plant invasions
are rarely considered. Selective foraging by deer, small mammals,
or insects on native rather than invasive vines could, in part,
explain the higher growth and abundance of invasives relative to
natives. We conducted an insect and mammal herbivore exclusion
experiment over two growing seasons to explore the amount of
damage and the effect of herbivore exclusion on the growth of 12
species of vines. We used vines from four families where each family
has one member that is a successful invader, one member that is
naturalized, and one native species (Table 1). To examine tolerance
to herbivory, we then conducted a simulated herbivory experiment
Family
Species
Plant origin
Caprifoliaceae
Lonicera japonica Thunb.
Lonicera caprifolium L.
Lonicera sempervirens L.
Celastrus orbiculata Thunb.
Euonymus fortunei (Turcz.) Hand.-Maz.
Celastrus scandens L.
Clematis terniflora DC.
Clematis florida Thunb.
Clematis virginiana L.
Ampelopsis brevipedunculata (Maxim.) Trautv.
Parthenocissus tricuspidata (Sieb. & Zucc.) Planch.
Vitis labrusca L.
Invasive
Naturalized
Native
Invasive
Naturalized
Native
Invasive
Naturalized
Native
Invasive
Naturalized
Native
Celastraceae
Ranunculaceae
Vitaceae
170
Table 1 The 12 temperate vine species used
in this study. Invasive vines as those listed as
invasive species in the USDA national plants
database (USDA-NRCS, 2001). We follow the
terminology of Pysek et al. (2004). Naturalized
plants are defined as those species that are
exotic and found outside cultivation in the
north-eastern USA but are not common
(Gleason & Cronquist, 1998). All naturalized
vines were introduced to the USA over 70 years
ago (Wyman, 1969).
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
Resistance and tolerance of invasive vines
in a greenhouse. With these experiments we tested two specific
hypotheses: (1) invasive vines are more resistant to herbivory
than native and naturalized vines and (2) invasive vines are
more tolerant of herbivory than native and naturalized vines.
METHODS
Field experiment
To examine how resistance and tolerance may affect the invasion
dynamics of woody vines in the north-eastern USA, we conducted an herbivore exclusion experiment on the grounds of the
Brookhaven National Laboratory (BNL), 40°52.1′ N, 72°51.7′ W,
between May 2003 and August 2004. Vine seeds of all 12 species
(Table 1) were purchased from Sheffield’s Seed Company, Inc.
(Locke, NY, USA). Seeds were cold stratified in fall of 2002 and
then planted and germinated in the greenhouse in March 2003.
The seedlings were grown in cones (Stuewe & Sons Inc, Corvallis,
OR, USA) in the State University of New York at Stony Brook
greenhouse until being planted on 22 and 23 May 2003. Seeds
from four species, Eunoymus fortunei, Lonicera japonica, Lonicera
sempervirens, and Lonicera caprifolium did not germinate. Cuttings
were used for E. fortunei, L. japonica, and L. sempervirens.
Because of limited material, we removed L. caprifolium from the
field experiment. For cuttings, plant material was cut using a
razor blade to include two nodes, the tip was dipped in rooting
hormone (Hormodin 1, MSD-Agvet, Rahway, NJ, USA), and the
cuttings were rooted in perlite (The Schundler Company,
Metuchen, NJ, USA). After approximately 2 weeks the rooted
cuttings were transferred to cones.
In May 2003, seedlings or cuttings were planted within a large
old field at BNL. Native vegetation in the old field was cleared in
the 1960s and early 1980s. After the clearing, the field was planted
with Dactylis glomerata L. and used for ecological studies in the
mid-1980s. Since then woody encroachment has been limited by
periodic mowing (Throop, 2005). The current vegetation is a mix
of old field species including Artemisia vulgaris L., Schizachyrium
scoparium (Mich X) Nash, Asclepias spp., and D. glomerata. The
old field is surrounded by matrix of mixed oak–pine community
dominated by Pinus rigida P. Mill. (pitch pine) and Q. alba L.
(white oak), and woody vines, such as Vitis labrusca, Lonicera
japonica, and Parthenocissus tricuspidata, are common along the
edge of the field. Numerous mammalian herbivores are present
on the site including white-tailed deer (Odocoileus virginianus),
woodchucks (Marmota monax), and eastern cottontail rabbits
(Sylvilagus floridanus). Deer are particularly abundant. It is
recommended that to avoid effects of over-browsing in northeastern forests deer density should remain below five deer per
square kilometre (Pennsylvania Game Commission, 2003). A
recent census of the Brookhaven National Laboratory property
estimates that there are 39 deer per square kilometre (Naidu,
1999).
The vines were planted within the field into one of 24 1.05 m ×
1.05 m plots divided among six blocks, where each block was
separated by approximately 50 m. Within each block, four treatments were randomly assigned in a split-plot design: caged,
caged and insecticide, uncaged and insecticide, and uncaged. To
reduce herbivory with minimal impact on light environment,
2.1-m-high polypropylene deer fencing with a 4.5-cm-wide
mesh was used. In addition to the fencing, hardware cloth was
sunk into the ground 30 cm and extended above the ground by
60 cm to prevent rodents from entering the plots. To remove
insect herbivores, half the plots were sprayed with Ortho Bug-BGone (3% esfenvalerate; Solaris-Scotts, San Ramon, CA, USA)
every 2 weeks. All other plots were sprayed with an equal quantity
of water.
Two to three replicates per species were planted in each plot
randomly within 36 spots within a 6 × 6 planting grid where each
plant was separated from the edge of the subplot and other seedlings
by 15 cm. A 1.5-m bamboo stake was placed in the ground adjacent
to each vine. Care was taken to ensure that all vines were touching
their respective stakes to allow for climbing. At the time of planting, leaf number, leaf length of the youngest fully expanded leaf,
and height were recorded to estimate initial size of all seedlings.
We tested our first hypothesis that invasive vines are more
resistant to herbivory in two ways. First, we examined differences
in biomass in the presence or absence of herbivores by harvesting
plants at three times: after one growing season (September
2003), after 1 year (May 2004), and after two growing seasons
(August 2004). At each harvest, two complete blocks were chosen
randomly for removal. For the first two harvests, above- and
below-ground biomass was collected. Because of the difficulty in
removing the extensive root systems, only above-ground biomass
was collected at the last harvest. All harvested plants were dried at
60 °C and weighed.
Second, we examined the amount of damage that invasive,
native, and naturalized vines experienced in the field. At the time
of planting, one young fully expanded leaf on each plant was
randomly selected and tagged using light wire tags on the petioles.
Herbivore damage was estimated by visually inspecting the
tagged leaves and recording the percentage of foliar damage every
4 weeks through the first and second growing season (Filip et al.,
1995). Mammalian herbivores often removed whole leaves or
branches, and in such cases where the entire leaf was missing
foliar damage was scored as 100%. After estimating damage, the
tag was removed and placed on a new fully expanded leaf.
Greenhouse experiment
To test the hypothesis that invasive vines are more tolerant of
herbivory than native or naturalized vines, we estimated plant
tolerance under more controlled conditions by conducting a
greenhouse experiment where mammal herbivory was simulated
by manually clipping plants. Vine seeds were purchased from
Sheffield’s Seed Co. (Locke, NY, USA), cold stratified for 30–
90 days, and germinated in the spring of 2004. On 25 May 2004,
12 seedlings of each species were transplanted into 3.79-L pots
(19.7 cm diameter and 17.8 cm deep) in a media of Pro-Mix BX
(Premier Horticulture Inc., Red Hill, PA, USA) and placed in the
Stony Brook greenhouse. A bamboo stake with a height of 1 m
was placed in the centre of each pot, and one plastic tie was used
to train the vine to the stake. Due to poor germination, the final
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
171
I. W. Ashton and M. T. Lerdau
design consisted of three seedlings of Clematis terniflora, 12 cuttings
each of Euonymus fortunei, Lonicera caprifolium, L. japonica, and
L. sempervirens, and 12 seedlings of each of the remaining six
species. Plants were placed randomly into one of six blocks and
allocated to one of two treatments: control or clipped.
All seedlings were fertilized after 1 week of growth and watered
as necessary over the course of the experiment. After 6 weeks of
growth, the number of leaves and the number of branches were
measured on all plants and one third of the plants were harvested, dried, and weighed. Stems were then clipped manually
using dull scissors on half of the remaining live plants. Approximately 50% of their leaves were removed and the removed biomass was distributed proportionally by clipping across all stems
to simulate grazing. To do this, the total number of leaves was
determined, divided by the number of main branches on each
vine, and then the branches were cut to include that number of
leaves. When there was clearly a dominant stem, the majority of
leaves were taken from that stem. On all plants across four of the
blocks, measurements of branch number, branch form (primary,
secondary, tertiary), and leaf number were repeated at weeks 0, 1,
2, 3, and 7 after the imposed clipping. After 13 weeks (7 weeks
after the clipping treatment), plants from five of the six blocks
were harvested, dried at 60 °C, and weighed. Roots were washed
prior to drying and weighed separately.
Data analyses
All data were analysed using linear mixed effects models (lme) in
R (2.4.0, 2006). Models with the best fit were found using AIC
criterion and likelihood ratio χ2 test was employed for tests of the
random effects. The likelihood ratio χ2 tests the hypothesis that
the variation due to the random effect is > 0, and is a one-sided
single degree of freedom test (Littell et al., 1996). Residuals were
visually inspected prior to analyses, data were transformed when
necessary to meet assumptions of normality, and post-hoc tests
were done using Bonferroni corrected Tukey HSD tests.
To examine the effect of plant origin on resistance to herbivory
in the field, we analysed relative growth rates and foliar damage
rates of all vines. Relative growth rates (RGR) were calculated
using initial estimates of mass based on regressions of seedling
height, leaf number, and leaf length and final above-ground biomass harvests as (loge final weight – loge initial weight)/(number
of days) (Hunt, 1990). RGR was analysed with caging treatment,
insect exclusion, plant origin (invasion status), and harvest date
as fixed effects with plant family, seed source, plant species,
block, and plot as random effects. Block effects were dropped
from the final model because they did not account for a significant source of variation. Monthly measures of percentage foliar
damage were analysed using a repeated measure linear mixed
model with cage treatment, insect exclusion, plant origin, and
time as main effects and block, plot, family, species, and individual as random effects. Foliar damage was arcsine squared-root
transformed prior to analyses and an autoregressive correlation
structure was found to be the best fit for the model.
Tolerance was estimated for both the field and the greenhouse
as the difference in RGR between damaged and undamaged
172
plants (Strauss & Agrawal, 1999). For these experiments, we
compared RGR of the damaged plants to the average growth of
the undamaged plants within the same harvest (field experiment) or block (greenhouse). In both cases, we tested for the
main effects of plant origin and harvest (for field only), and family, species, and block were included as random effects. In the
field, the best fit model did not include family. In the greenhouse
experiment, family, block, and species did not account for a significant source of variation, and the best fit model included only
plant origin. Positive tolerance values indicate increased growth
due to damage, values of zero indicate compensation and no net
change in growth rate, and negative values indicated that RGR of
damaged plants is less than that of undamaged plants.
Finally, to elucidate the mechanisms responsible for tolerance
in the greenhouse, we also tested for effects of clipping treatment
and plant origin on RGR, root:shoot (RS ratio), leaf number, and
branching patterns. RGR of plants in the greenhouse experiment
were calculated as above using the average dry mass of the plants
harvested at the time of clipping as initial size estimates of each
species and final biomass included above- and below-ground
components. For RGR and RS ratio, the main effect of plant origin
and clipping treatment was tested and block, plant family, and
species were random effects. To examine the effect of the clipping
treatment on leaf and branch number, we calculated the log response
ratio to the treatment for all species where the response =
log (damaged number/undamaged number). Positive responses
indicate that the clipped plant had a greater number of leaves or
branches than the undamaged control, responses equal to zero
show no effect of clipping, and a negative number indicates a
reduction in leaf or branch number caused by clipping. Weekly
measures of log response ratios of branch and leaf number were
analysed using repeated measures analyses with plant origin and
week as main effects and block, family, and species as random
effects using an autoregressive correlation structure.
RESULTS
Resistance to herbivory in the field
The four native vines grew significantly slower than naturalized
and invasive vines during the first growing season (Fig. 1). However,
after this time, RGR of all vines declined, and differences among
invasives, natives, and naturalized vines were no longer significant
(Fig. 1). Vines grew faster in the absence of mammal herbivores (cage
effect: F1,6 = 20.4, P = 0.004), regardless of plant origin (cage ×
plant origin: F2,103 = 0.7, P = 0.503) where growth rates within
cages were more than twice that of the plants subjected to herbivory (0.024 ± 0.002 log mg day–1, n = 277, and 0.009 ± 0.001,
n = 232, respectively). The insect exclusion treatment caused no
difference in growth overall (spray effect: F1,6 = 0.07, P = 0.798),
and plant origin did not determine this response (spray × plant
origin: F2,103 = 1.3, P = 0.280). Differences in RGR among plant
families (χ1 = 24.0, P < 0.001) and species (χ1 = 55.1, P < 0.0001)
accounted for a significant amount of variation in the statistical
model where some families and species grew much faster than
others (Table 2). The vines in the Caprifoliaceae were much
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
Resistance and tolerance of invasive vines
the end of the growing season (Fig. 2). Foliar damage rates on vines
grown in the caged plots were minimal compared to those outside
cages (6.2 ± 0.55 and 38.5 ± 1.28%, n = 2500, respectively), regardless
of plant origin (Fig. 2). The insect exclusion treatment did not
significantly decrease foliar damage rates (F1,508 = 1.5, P = 0.215)
and this was consistent across plant origin (F2,508 = 0.8, P = 0.458).
In addition to the effects of season and caging, there was an interactive effect of plant origin and time where native vines showed
more damage by the end of the season than invasive (F7,1818 = 3.7,
P = 0.0006) or naturalized vines (F7,1405 = 2.7, P = 0.0095), particularly in the caged plots (Fig. 2a,b). Naturalized vines experienced lower rates of leaf damage than both natives (F1,26 = 18.8,
P = 0.002) and invasives (F1,26 = 5.2, P = 0.031) over the length of the
experiment and across treatments. Similar to growth rates, we
also found some variation in damage rates among plant families.
The vines in the Celastraceae (13 ± 1.1%, n = 1400) experienced less
damage than the Caprifoliaceae (29 ± 2.0%, n = 832), Ranunculaceae
(25 ± 1.8%, n = 1080), and Vitaceae (24 ± 1.39%, n = 1728).
Tolerance to field and simulated herbivory
Figure 1 Relative growth rates of field grown invasive, native,
and naturalized vines under four herbivore exclusion treatments
harvested after (a) one growing season, (b) 1 year, and (c) at the
end of two growing seasons. Error bars represent ± SE. ***P < 0.001,
**P < 0.01, *P < 0.05 and reported statistics refer to all panels.
All plant origins increased growth rates in the mammal herbivore
exclosures (no significant effect of cage × plant origin), and insect
exclusion treatments did not affect growth rates.
larger by the final harvest date (mean = 29.7 ± 7.83 g) than vines
in the Ranunculaceae (mean = 5.1 ± 2.1 g), Celastraceae (mean
= 3.9 ± 2.1 g), or Vitaceae (mean = 3.8 ± 2.2 g).
Foliar damage rates varied significantly throughout the duration
of the experiment and, in both years, reached a maximum towards
Woody vines, regardless of plant origin, growing season, or plant
family (χ1 = 3.6, P = 0.0566) were unable to fully compensate for
damage caused by mammals in the field relative to caged plants
(Fig. 3). Herbivores had the largest effect on vines during the initial
growing season (Fig. 3). In general, vines grew much faster in the
greenhouse than the field (Table 2).
Contrary to results from the field experiment, invasive vines
were more tolerant of simulated herbivory in the greenhouse
than either native or naturalized vines (Fig. 4), where again, there
was no significant variation among families in measured tolerance
(χ1 = 0.22, P = 0.6342). Consistent with the tolerance results, there
was a significant interactive effect of plant origin and clipping on
RGR (F2,43 = 3.4, P = 0.042) and RS ratio (F2,43 = 4.0, P = 0.026)
where invasives showed no response to clipping but naturalized
and native vines decreased growth rates (Table 2) and increased
allocation to roots from 0.4 ± 0.04 to 0.6 ± 0.07 and from 1.0 ± 0.20
to 1.2 ± 0.16, respectively, when clipped (Table 2b).
During the 7 weeks following the clipping treatment, clipped
invasive vines increased the number of leaves (Fig. 5a) relative to
the undamaged plants. Native and naturalized vines, however,
were unable to compensate for clipping and by the seventh week,
the clipped plants still had fewer leaves than the undamaged
plants (Fig. 5a). All vines increased the number of branches after
clipping, but the relative increase in branch number was greatest
for native and invasive vines (Fig. 5b). In three of the plant families
we examined, the clipped invasive vines had the most branches.
The invasive Celastraceae, in particular, increased branch number
relative to the native and naturalized vine. In the Ranunculaceae, it
was the native that consistently had more branches than its relatives.
DISCUSSION
To examine the role that resistance and tolerance play in the success
of temperate vine invasions, we tracked variation in relative
growth rates and herbivore damage of 12 phylogenetically related
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
173
I. W. Ashton and M. T. Lerdau
Table 2 The effect of herbivore damage and environment on (a) mean relative growth rates (RGR; log mg day–1) and (b) root to shoot ratio (RS)
of 12 species of temperate vines. Error bars represent ± SE and sample sizes are indicated in parentheses below the species and refer to each
respective experiment.
(a) RGR
Origin
Caprifoliaceae
L. japonica (33,32,4,3)
L. caprifolium (3,3)
L. sempervirens (13,15,4,3)
Celastraceae
C. orbiculata (28,31,5,5)
E. fortunei (13,16,5,5)
C. scandens (28,30,5,5)
Ranunculaceae
C. terniflora (8,13)
C. florida (8,11,5,5)
C. virginiana (28,34,5,5)
Vitaceae
A. brevipedunculata (26,29,5,5)
P. tricuspidata (23,34,5,5)
V. labrusca (24,32,5,5)
Field
(b) RS
Field: no mammal Greenhouse:
herbivores
clipped plants Greenhouse
Greenhouse:
clipped plants Greenhouse
Invasive
0.016 ± 0.0026 0.038 ± 0.0059
Naturalized na
na
Native
0.006 ± 0.0057 0.030 ± 0.0058
0.053 ± 0.0033 0.058 ± 0.0011 0.3 ± 0.02
0.028 ± 0.0079 0.038 ± 0.0066 0.4 ± 0.03
0.025 ± 0.0022 0.034 ± 0.0043 0.3 ± 0.02
0.4 ± 0.02
0.4 ± 0.07
0.4 ± 0.06
Invasive
Naturalized
Native
0.010 ± 0.0022 0.020 ± 0.0031
0.010 ± 0.0039 0.005 ± 0.0036
–0.004 ± 0.0014 0.002 ± 0.0012
0.043 ± 0.0036 0.040 ± 0.0020 1.1 ± 0.19
0.015 ± 0.0053 0.024 ± 0.0025 0.6 ± 0.05
0.026 ± 0.0054 0.045 ± 0.0073 1.6 ± 0.18
1.4 ± 0.07
0.6 ± 0.08
1.3 ± 0.6
Invasive
Naturalized
Native
0.018 ± 0.0094 0.020 ± 0.0059
0.017 ± 0.0071 0.023 ± 0.0079
0.020 ± 0.0043 0.032 ± 0.0055
na
na
na
0.034 ± 0.0057 0.048 ± 0.0071 0.9 ± 0.14
0.046 ± 0.0032 0.053 ± 0.0045 0.8 ± 0.08
na
0.5 ± 0.08
0.5 ± 0.10
Invasive
0.002 ± 0.0016 0.029 ± 0.0052
Naturalized
0.017 ± 0.0049 0.033 ± 0.0062
Native
–0.0001 ± 0.0017 0.018 ± 0.0037
0.032 ± 0.0016 0.033 ± 0.0037 2.1 ± 0.24
0.035 ± 0.0033 0.037 ± 0.0013 0.5 ± 0.11
0.039 ± 0.0030 0.044 ± 0.0034 1.9 ± 0.23
1.8 ± 0.26
0.3 ± 0.04
1.4 ± 0.19
na, not available.
Figure 2 The foliar damage rates (%) of
invasive, native, and naturalized vines in
(a) mammal exclosure cages and sprayed
with insecticide, (b) mammal exclosures,
(c) uncaged and sprayed, and (d) uncaged
control conditions. Error bars represent ± SE,
***P < 0.001, **P < 0.01, *P < 0.05,
ns = P > 0.05.
174
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
Resistance and tolerance of invasive vines
Figure 3 The effect of time and plant origin on the tolerance of
vines to mammal herbivory in the field. A tolerance below zero
indicates that undamaged plants grew faster than damaged plants,
and smaller values indicate less tolerance to herbivory. Different
letters indicate significant differences and error bars represent ± SE;
*P < 0.05, ns = P > 0.05.
Figure 4 The effect of plant origin on tolerance to simulated
mammal herbivory of 12 species of vines grown in a greenhouse.
Different letters indicate significant differences and error bars
represent ± SE; *P < 0.05.
Figure 5 The relative effect of clipping on
(a) leaf number and (b) branch number of
invasive, native, and naturalized vines during
the 7 weeks following treatment. Positive log
response ratios indicate that the clipped plant
had a greater number of leaves or branches
than an unclipped control. Clipping treatment
was conducted just following week zero
measurements ***P < 0.001, **P < 0.01,
ns = P > 0.05.
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
175
I. W. Ashton and M. T. Lerdau
vines in a field herbivore-exclusion and a greenhouse-simulated
herbivory experiment. We predicted that invasive vines would be
more resistant and tolerant to insect, mammal, and simulated
herbivory than their naturalized relatives.
Resistance to herbivory in the field
Our field results did not support the hypothesis that invasive
vines are more resistant to herbivory than native and naturalized
vines. Over the two growing seasons, all vines were damaged to
some degree, regardless of origin, suggesting that no species is
fully ‘escaping’ herbivores, particularly generalist herbivores,
such as deer. As expected, however, we found that native vines
were less resistant to insect and mammalian herbivores than naturalized and invasive vines and experienced higher rates of foliar
damage at the end of each growing season (Fig. 2). It is possible
that the low resistance in natives may be due to a higher load of
specialist herbivores. Whether due to specialists or generalists,
the increased damage rates translated into lower growth rates of
natives compared to naturalized and invasive vines only during
the first season; by the second season growth rates were equivalent among native, naturalized, and invasive vines.
Contrary to our hypothesis and previous work that has shown
naturalized plants typically suffer greater herbivory than invasive
plants (Cappuccino & Carpenter, 2005), we found that naturalized
vines, not invasive vines, had the lowest foliar damage rates.
Since naturalized vines did not respond to this relaxation of
herbivore pressure by increasing growth rates, we expect that the
growth rates of these naturalized vines are limited by factors
other than herbivores. In the case of the naturalized Celastraceae,
Euonymus fortunei, the leaves are thicker than its relatives which
could provide herbivore resistance at a cost of slow growth. In the
three other naturalized vines, there was no apparent difference in
the leaf structure, but it is possible that other architectural or
chemical traits provide resistance. Our experiment suggests that
resistance alone cannot explain invasion success because differences
in herbivory did not translate into differences in growth, and
naturalized vines had lower rates of damage than natives (rates
comparable to those of invasives) and yet were not invasive.
Plant resistance and growth rates varied over the course of the
experiment and, in general, herbivore damage increased over
each growing season and over the 2 years (Fig. 2). Previous studies
have also found variation in herbivore resistance with time
(Agrawal et al., 2005) and such changes may be crucial to the
invasion process. When herbivore loads are high on native plant
communities this may provide ‘invasion opportunity windows’
(Johnstone, 1986; Agrawal et al., 2005). For instance, Clematis
virginiana, a native, suffered high rates of defoliation within the
cages during July of each year but its naturalized relatives
remained fairly undamaged. Also, during the first summer, when
the plants were seedlings, natives had the highest damage and
lowest growth rates. If native vines generally suffer higher rates of
herbivory at the seedling stage, it could suggest that invasive and
naturalized vines can establish more easily than natives.
While there was some variation in resistance over time, vines
generally had low growth rates and high damage rates outside the
176
exclosures. This suggests that deer on eastern Long Island may
play an important role in restricting vine invasions through their
consumption of young vines. White-tailed deer are known to
strongly impact native plants (Russell et al., 2001; Rooney &
Waller, 2003), and our results suggest a major role for mammals
in affecting non-native plants as well. Deer populations in this
area are at historically high levels because of habitat changes and
hunting suppression (Naidu, 1999). The explosion of deer populations is widespread across the eastern USA and is perceived to be
ecologically deleterious; however, deer may be one of the last
bulwarks preventing more substantial vine invasions of these
ecosystems. Other studies have shown that native generalist
herbivores, particularly mammals, are providing biotic resistance
to not only vines, but also to many other plant invasions across a
diversity of ecosystems (Parker et al., 2006).
Tolerance to herbivory
Consistent with our second hypothesis, invasive vines were more
tolerant of simulated herbivory than native or naturalized vines
in the greenhouse (Fig. 4). Some invasives, such as Celastrus
orbiculata, overcompensated for damage and had higher growth
rates after clipping (Table 2a). There are numerous mechanisms
that allow for plants to grow new tissue after loss to herbivores
(Marquis, 1992; Strauss & Agrawal, 1999; Tiffin, 2000). In this
experiment, we explored only the ability of vines to reallocate
root stores to above-ground tissue and how this reallocation is
reflected in architectural changes (leaf number and branch
number). By quickly replacing above-ground tissue, invasive
vines were able to maintain a similar RS ratio after damage while
RS ratio of native and naturalized vines increased after damage
(Table 2b). Increased branching and release of apical dominance
may be essential in allowing vines to compensate for damage and
increasing leaf number may be a particularly effective mechanism allowing invasive vines to tolerate damage (Fig. 5).
Unlike the greenhouse, in the field we found that tolerance
only varied with time and not plant origin (Fig. 3). As explained
above, naturalized vines suffered the lowest foliar damage rates
(Fig. 2), however, despite these low damage rates, there was
no difference in growth in the field among invasive, native, and
naturalized vines (Table 2; Fig. 1). One explanation for this may be
that invasive and native vines are more tolerant of herbivores
than naturalized vines. But, in the field, none of the vines were
capable of replacing the lost tissue and compensating for the
damage caused by mammal herbivores. The high resource conditions in the greenhouse, lack of plant competition, the lower total
foliar damage (only 50% compared to up to 80% in the field),
or the difference between chronic and acute damage may have
permitted greater tolerance in the greenhouse. Our greenhouse
results are consistent with previous work comparing herbivore
response in the field between the native, Lonicera sempervirens,
and invasive, Lonicera japonica, where the invasive was found to
have higher tolerance than the native (Schierenbeck et al., 1994).
While the results from the greenhouse experiment were not consistent
with our field results, our experiment adds to a growing number
of studies that suggest compensatory growth and tolerance may
© 2007 The Authors
Diversity and Distributions, 14, 169–178, Journal compilation © 2007 Blackwell Publishing Ltd
Resistance and tolerance of invasive vines
be critical to the success of invasive plants (Kimball & Schiffman,
2003; Rogers & Siemann, 2003, 2004; Bossdorf et al., 2004;
Stastny et al., 2005).
Conclusions
In summary, we found that (1) differential resistance to herbivory
does not explain invasion success in these vines, (2) tolerance to
herbivory does correlate to invasion success in these vines, and
architectural changes and shifts in root to shoot allocation may
underlie this pattern (3) on a community scale, deer and other
generalist herbivores may be suppressing plant invasions on
Long Island and perhaps also in other areas where deer populations are high. Therefore, herbivory may modulate the success of
vines by reducing their establishment and growth in the field.
However, while most studies of invasive plants and natural enemies
have focused on resistance, this work suggests that tolerance may
also play a large role in facilitating invasions.
ACKNOWLEDGEMENTS
This manuscript was greatly improved by the comments from
Geeta, V. Eviner, C. Janson, and J. Gurevitch. Thanks to A. Levy,
K. Howe, J. Hickman, and S. Uihlein for help with fieldwork.
This work was supported by a grant from USFWS Upton Preserve
(IA and MTL) and a NASA Earth System Science Fellowship
(IA).
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