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RESEARCH ARTICLE

Prey Capture Success by Established


and Introduced Populations of the
Venus Flytrap (Dionaea muscipula)
John J. Hutchens, Jr. and James O. Luken
ABSTRACT
We examined whether the ecological function (i.e., prey capture) of a rare, endemic carnivorous plant, Venus flytrap
(Dionaea muscipula), was maintained in managed habitats along the sand rims of Carolina bay wetlands at a preserve in
the coastal plain of South Carolina, U.S.A. We hypothesized that prey capture would be similar between established and
introduced plants because environmental conditions were similar. Number of traps, trap length, trap width, and prey
length did not significantly differ between introduced and established populations, and most indicators of prey capture
success significantly favored plants growing in introduced sites. Plants in introduced sites had almost 10% more closed
traps, had significantly more traps with prey, had more traps with multiple prey items, and had a greater proportion of
closed and total traps containing prey. When combined across sampling dates, ants and spiders composed the majority
of captured invertebrates; spiders predominated in established sites while ants predominated in introduced sites. Prey
availability on one date at a subset of sites was significantly greater in introduced sites. Our data supported the effectiveness of the clearing and transplanting restoration activity for Venus flytraps by showing that individual plants growing in
introduced sites have similar structure and function as those in established sites. Consistently greater prey capture success by introduced plants likely contributed to their growth, although underlying reasons for differences in prey capture
between introduced and established plants remain uncertain. Evaluating prey capture of carnivorous plant populations
provides insight into mechanisms underlying restoration success.
Keywords: carnivorous plant, Carolina bay, ecological function, restoration

ttempts to stem losses of biodiversity have led to several restoration approaches including moving species
to new, suitable habitats. Successfully introducing plants not
only requires knowledge of requirements for light, water,
and nutrients, but also familiarity with interactions that
might occur with other species (e.g., herbivory, pollination,
mycorrhizae). Pollination within the context of restoration
has begun to receive needed attention (Menz et al. 2011);
nevertheless, underlying reasons for success of plant reintroductions are poorly understood and often not studied
(Godefroid et al. 2011). Restoration of carnivorous plant
populations presents added complexity beyond pollination
because consideration of successful capture of invertebrate
prey also is necessary. Carnivorous plants face a variety
of threats, the foremost of which is habitat loss (Jennings
and Rohr 2011); introductions into new habitats are an
important conservation tool (Jennings and Rohr 2011).
Ecological Restoration Vol. 33, No. 2, 2015
ISSN 1522-4740 E-ISSN 1543-4079
2015 by the Board of Regents of the University of Wisconsin System.

Restoration practices often are described as being limited


to replacement of ecological composition and structure
at the expense of ecological function (Hobbs and Norton
1996; but also see Wortley et al. 2013). Function is often
ignored because it is assumed that if composition and
structure are replaced, then function will be restored without further action. In fact, ecological function may be lost
in these habitats even though structure is restored. For
example, restored California salt marshes did not function as nesting habitat for the endangered light-footed
clapper rail because the presence of introduced plants (the
structure) in constructed marshes were not dense enough
to support rail nests (the function; Zedler 1993). Here, we
examined whether the function (prey capture) of a rare,
endemic carnivorous plant, Venus flytrap (Dionaea muscipula), was restored in managed habitats along the sand
rims of rare Carolina bay wetlands.
Carnivorous plants growing in nutrient-poor environments are hypothesized to depend on frequent fires to
create full-sun environments (Givnish et al. 1984). However, forest management using prescribed fires to mimic
natural fires is often limited by safety concerns. One
June 2015 ECOLOGICAL RESTORATION33:2 171

potential remedy for this concern is to use mechanical


clearing. For example, clearings made by large mowers on
the rims of Carolina bays provided an effective, short-term
habitat for establishing Venus flytrap populations (Luken
2005). Similarly, reductions in competitors by clipping
and weeding resulted in positive responses to a species
of pitcher plant in seepage bogs (Brewer 1999, 2003). By
contrast, a similar restoration treatment failed to elicit
equivalent plant responses for a different pitcher plant
species (Brewer 2005) because of limited availability of
moist sites for germination (Chesser and Brewer 2011).
An additional factor affecting success of these restoration
activities is whether removal of nearby plants affects prey
capture by carnivorous plants. Whereas differences in prey
capture between restoration treatments were evaluated in
the above pitcher plant studies, the role of differential prey
capture success by flytraps in the restoration activity by
Luken (2005) is unknown.
Our overall objective was to evaluate prey capture of
Venus flytraps in mowed openings (i.e., managed habitats)
on Carolina bay ecotones. Flytraps had been introduced
into these openings by transplanting adults and sowing
seeds (Luken 2005). We hypothesized that flytrap function
(i.e., prey capture) would be similar in managed habitats compared to nearby habitats containing established,
resident flytraps because after two years, introduced adult
plants had high survivorship and high flowering percentages and seedlings germinated from seeds survived (Luken
2005). We compared prey capture of introduced populations in the managed habitats with that previously reported
for nearby established populations (Hutchens and Luken
2009). Prey availability in established and managed habitats also was assessed to elucidate a possible mechanism
underlying differences in flytrap function.

Methods
Study Site and Restoration Treatment
Venus flytraps were studied at Lewis Ocean Bay Heritage
Preserve (LOBHP) in Horry County, South Carolina U.S.A.
(3347'N, 7852'W), a 3640-ha protected area that includes
22 Carolina bays and extensive pine savanna. LOBHP is
managed with frequent prescribed burning and occasional
understory cutting.
Portions of rims of two Carolina bays intersecting a
power line corridor that crosses LOBHP were manipulated
for Venus flytrap restoration in May 2003 (Luken 2005).
Previously, Venus flytraps had been found in power line
corridors intersecting LOBHP Carolina bays. Briefly, nine
10 20m sites were mowed using a mechanical mower
and cleared to remove dense evergreen shrubs and trees
(e.g., Pinus serotina, Persea palustris, and Gordonia lasianthus). Root mats were removed from two 0.5-m2 plots

172 June 2015 ECOLOGICAL RESTORATION33:2

within each site, leaving bare soil with no soil amendments.


Venus flytraps were introduced by seed into one plot and
adults were transplanted into an adjacent plot. After two
years, transplanted flytraps showed high survivorship, flytrap seedlings persisted at low densities, and several suppressed flytraps regrew at each site. Additional details of
the restoration methods and results are in Luken (2005).

Data Collection
Sampling was conducted as part of a related study investigating diet of Dionaea in established populations (Hutchens and Luken 2009). Ten populations of Dionaea in established sites and six populations in introduced sites were
sampled in winter (4 February 2006), spring (17 May 2006),
and autumn (26 October 2006). Sampling in summer was
omitted because plants were dormant due to drought.
Within each population, two Venus flytraps in each of
three size classes were selected for prey assessment (total n
= 60 plants per sampling date, except for spring when two
plants in the largest size class in one established population were unavailable). Although individual plants were
selected randomly, plants had to have at least one closed
trap in order to be selected. Sampling of captured prey in
the field was guided by petiole length on individual plants,
a leaf characteristic correlated with trap length (Hutchens
and Luken 2009). Size classes consisted of (1) petioles
(=phyllodes) <1cm long, (2)petioles >1 and <2cm long,
and (3)petioles >2cm long. These size classes spanned
the typical size range of Venus flytraps at LOBHP (Luken
2007). On each plant, the numbers of open and closed traps
were counted. Closed traps were removed from petioles and
preserved in 95% ethanol. In the laboratory, trap length,
trap width and prey length (if present) were measured to
the nearest mm using electronic calipers and a dissecting
microscope with a stage micrometer, respectively. Prey
items were usually identified to order, although ants (Formicidae) were distinguished from Hymenoptera because
of their abundance. Identification was sometimes limited
by specimen decomposition within traps.
Prey availability was assessed at the six introduced sites
and at six randomly chosen established sites. Two unglazed
clay tiles (10.8cm 10.8cm) with adhesive (Tangle-Trap,
The Tanglefoot Company, Grand Rapids, MI, USA) applied
to one surface were set on the ground amid flytraps at
each of the twelve sites on 11 May 2010. Six days later,
tiles were collected and returned to the laboratory where
attached invertebrates were identified, counted, and body
length measured as above. While this survey was limited
in spatial and temporal replication compared to the prey
capture study, we hoped the survey would help distinguish
between differences related to flytrap function and those
related to site characteristics.

Table 1. Mean (SE) values for each parameter describing Venus flytrap (Dionaea muscipula) prey acquisition by treatment and date of collection at Lewis Ocean Bay Heritage Preserve, South Carolina, US. All data (except for total
traps with multiple prey) were calculated for individual plants and analyzed statistically using a nested randomized
block analysis of variance using date of collection as the block. F-values for the treatment effect were calculated
using the mean square error from sites nested in treatment. Total traps with multiple prey were calculated for individual sites and compared between treatments using a randomized block analysis of variance of the total traps per
site. Means by date are not shown because our primary focus was on differences by treatment.
Parameter
Total number of traps
Total number of traps with prey2
Total number of traps with multiple prey2
% of total traps closed4
% of total traps with prey4
% of closed traps with prey4
Mean trap length (mm)1
Mean trap width (mm)1
Mean prey length (mm)1
1

Established

Treatment
Introduced

F1, 14

Date

7.1 (0.4)
1.6 (0.1)
1.7 (0.3)
46.3 (1.9)
23.8 (1.8)
51.0 (2.8)
13.1 (0.4)
7.8 (0.2)
4.6 (0.3)

6.8 (0.5)
2.2 (0.2)
3.0 (0.5)
55.1 (2.4)
35.0 (2.8)
62.4 (3.7)
14.3 (0.5)
8.8 (0.3)
3.9 (0.2)

0.20
9.35
6.673
9.87
15.41
7.12
0.98
2.65
0.05

0.658
0.009
0.013
0.007
0.002
0.018
0.338
0.126
0.827

F2, 262
44.32
20.06
5.01
9.27
13.53
8.55
5.94
2.31
0.785

p
< 0.001
< 0.001
0.011
< 0.001
< 0.001
< 0.001
0.003
0.101
0.459

Log10 transformed
Log10 + 1 transformed
F1, 43 because individual plants were not included as a result of prevalence of zeros
4
Arcsin-squareroot transformed
5
Error degrees of freedom = 224 because of plants without any prey
1
2
3

Data Analysis
Prey capture success was estimated using several measures:
total number of traps, total number of traps with prey,
total number of traps with multiple prey, percent of total
traps closed, percent of total traps with prey, and percent
of closed traps with prey. Plant size (trap length and width)
and prey size (body length) also were measured. These
measures were statistically compared between treatments
(i.e., introduced vs. established) using analysis of variance (ANOVA), General Linear Model in SYSTAT (Vers.
12, SYSTAT Software, Inc., San Jose, California, U.S.A.).
Statistical assumptions (i.e., normality and equal variance) were tested and appropriate transformations applied.
Although all plants were included in the statistical analysis,
we considered individual plants to be subsamples of the
true replicate, sites. As a result, sites were nested in the
treatment and this term, Sites(Treatment), was used as the
error term to calculate F for Treatment (Gotelli and Ellison
2004). Collection date was included in the ANOVA model
as a blocking factor because we were not as interested in
differences among dates as we were in incorporating seasonal variation in prey capture success for our evaluations
of the management treatment. Individual traps containing
multiple prey items had a high prevalence of zeros at the
level of an individual plant, so we summed the number
of traps with multiple prey items by site and statistically
compared these data between treatments using a randomized blocked ANOVA without including individual plants.
Captured prey assemblages in introduced and established populations were examined using ordination. We
calculated the relative proportion of the top fifteen invertebrate groups (see below) for each site across all three

sampling dates. Dates were combined to reduce seasonal


variation and to focus on patterns associated with the
treatment. Non-metric multidimensional scaling (NMDS)
was run using the slow and thorough setting in PC-ORD
(Version 5.15, MjM Software, Gleneden Beach, Oregon,
U.S.A.) and the Sorensen distance. Axes were tested for
significance using a Monte Carlo test with 250 runs, and
the relative abundances of individual taxa were correlated
with each axis using Pearsons product-moment correlation
to help explain the ordination.
Prey items collected on the two tiles at each site were
combined by site for statistical analyses. Differences in total
number of prey, total number of adult insects, and average
length of prey were compared between introduced and
established sites with two-sample t-tests.

Results
Most of our indicators of prey capture success were
higher for plants growing in the introduced sites (Table
1). Although individual plants in both treatments averaged
approximately seven traps, plants in introduced sites had
almost 10% more closed traps. Plants growing in introduced sites had significantly more traps with prey than
those in established sites, but the absolute difference was
relatively small (approximately one trap). The total number
of traps with multiple prey items per site also was greater in
introduced sites compared to established sites. The proportion of closed and total traps containing prey were 11 to
12% greater in introduced than in established sites. Trap
length, trap width, and prey length did not significantly
differ between treatments (Table 1).
June 2015 ECOLOGICAL RESTORATION33:2 173

Araneae

Formicidae

Coleoptera

Collembola

Unknown

Lepidoptera

Established
Introduced

Diplopoda

Hymenoptera

Orthoptera
Hemiptera
Chilopoda

Blattoidea

Diptera

Gastropoda
Acari
0.0

0.1

0.2

0.3

0.4

0.5

Proportion of total invertebrates in traps

Figure 1. Major taxonomic groupings as a proportion of total invertebrates


collected by Venus flytraps in established and introduced populations at
Lewis Ocean Bay Heritage Preserve, South Carolina, US.

1.5

Established

1.0

Introduced

Axis 2

0.5

0.0

0.5

1.0

1.5
1.5

1.0

0.5

0.0

0.5

1.0

1.5

Axis 1
Figure 2. Non-metric multidimensional scaling (NMDS) ordination of the
top fifteen invertebrate taxonomic groups caught by Venus flytraps for
each site across all three sampling dates. Symbols represent ordination
scores for established () and introduced () sites. Final stress = 13.8. Axis
1 was significant (p = 0.004) and explained 24.2% of total variation. Axis 2
also was significant (p = 0.040) and explained 58.3% of total variation.

When combined across the three sampling dates, ants


and spiders composed the majority of all captured invertebrates in established and introduced sites (Fig. 1). However,
the predominant taxon differed between treatments as spiders predominated in established sites while ants were most
important in introduced sites. Beetles also were important

174 June 2015 ECOLOGICAL RESTORATION33:2

in both treatments. Together, ants, spiders, and beetles


composed 69% and 73% of all captures in established and
introduced sites, respectively. Overall, fifteen orders of
invertebrates were identified (Figure 1; Isopoda not shown).
Two NMDS axes were found to be significant (Figure 2;
final stress = 13.8), with established sites primarily having

lower scores on Axis 1 (p = 0.004, explained 24.2% of total


variation) and higher scores on Axis 2 (p = 0.040, explained
58.3% of total variation) than introduced sites. Still, two
sites of each treatment plotted in similar ordination space
as the other treatment (Figure 2), indicating treatments
were relatively weakly separated. Axis 1 was positively correlated (Pearson correlation; R = 0.773) with ants. Axis 2
was positively correlated (Pearson correlation; R = 0.908)
with spiders and negatively correlated (Pearson correlation;
R = 0.819) with ants.
A total of 198 invertebrates were collected on tiles for the
prey availability survey, with prey composition dominated
by springtails (Collembola, 38%) and adult flies (Diptera,
30%). In contrast to prey items found in traps, ants composed only 4% of the total number collected, only one
spider was collected, and no beetles were caught. Mean total
abundance was significantly greater (Two-sample t-test; tcalc
= 2.244, p = 0.044, df = 12) in introduced (mean SE = 18.1
3.0 invertebrates) than in established sites (mean SE
= 10.1 1.9 invertebrates). No significant difference was
found between site types for adult insect abundance (Twosample t-test; tcalc = 0.191, p = 0.851, df = 12; introduced
mean SE = 5.9 2.0 invertebrates; established mean
SE = 5.4 1.0 invertebrates). Invertebrates collected on
tiles were small across sites, and were somewhat longer in
established sites (Two-sample t-test; tcalc = 2.078, p = 0.060,
df = 12; introduced mean SE = 1.0 0.1mm; established
mean SE = 2.0 0.5mm).

Discussion
Our data supported the effectiveness of clearing and transplanting (Luken 2005) by showing that individual plants
growing in introduced sites have similar structure and
function as those in established sites. Consistently greater
prey capture success by introduced plants likely contributed
to their growth, although underlying reasons for differences
in prey capture between introduced and established plants
remain uncertain.
Structural measures of individual flytraps were similar
between introduced and established populations in our
study. Two years after plant introduction, trap number
per plant (five to six) also was similar between introduced
populations and in two of the established populations
(Luken 2005). Our study three years after introduction
that included eight additional established populations
found all sampled plants averaged approximately seven
traps per plant. The same number of traps combined with
no significant differences in trap size (petiole length and
width were not recorded) between the two treatments indicate individual plants in introduced sites grew similarly to
plants in established sites. Conclusions about trap sizes in
the present study are limited, however, because we collected
data for the same number of individuals in three size classes
instead of collecting a random sample of plants at each site.

Prey capture represents a key ecological function of carnivorous plants. Introduced flytraps consistently had modestly higher prey capture success compared to established
flytraps. How ecologically important the roughly 10%
greater capture success was for flytrap success (i.e., growth)
is uncertain, but obvious differences in plant growth were
not evident (see above). Additional nutrients from more
prey are a likely benefit, but variation between population
types in the size and identity of captured invertebrates
may offset this advantage in prey number. No significant
difference in prey length was found, so it was unlikely that
more nutrients were available in larger prey for established
flytraps unless prey of the same size differed in nutrient
content. While prey assemblages differed in the identity
of the dominant taxon (spiders in established populations
and ants in introduced ones), other prey taxa were similar
in relative abundance and identity at the ordinal level.
Nitrogen content of spiders is approximately 11% (Fagan
et al. 2002), but varies more in ants because of diet differences (approximately 11% for herbivores and omnivores;
approximately 13% for predators; Davidson 2005). Schulze
et al. (2001) found prey of Venus flytraps to vary greatly in
stable nitrogen values, but that ants and spiders had similar
values. Overall, these lines of evidence lead us to conclude
that flytrap function in terms of prey collection and presumably nutrient collection were similar in introduced and
established populations.
Invertebrate availability based on invertebrates caught
on sticky tiles was higher in introduced sites compared to
established sites, suggesting that the moderately greater
prey capture success in introduced sites could have been
a function of greater prey availability. Carnivorous plants
collect prey at the same rate as they are available up to
a certain threshold (i.e., they have a Type I functional
response curve; Jeschke et al. 2004), which means that
flytraps likely can capture more invertebrates as more prey
become available (JJH, unpublished data). Furthermore,
data for prey caught by flytraps in their natural habitats
show little evidence that flytraps select larger prey by allowing smaller prey to escape as many prey items are only 1
mm in body length (Hutchens and Luken 2009), meaning
most additional invertebrates crawling across an open trap
have the same chance of being caught (but also see Gibson
and Waller 2009). Nevertheless, our survey of invertebrate
availability appeared inadequate in that the identity of the
collected invertebrates was dominated by springtails and
adult true flies whereas prey items captured by Dionaea
were dominated by ants and spiders. These taxonomic
differences may be a result of not enough adhesive being
placed on tiles, which allowed stronger invertebrates to
escape tiles. As no published data for terrestrial arthropods exist for our study site, these data only provide a first
attempt at characterizing prey availability and should be
treated with caution. More evaluation of abundances of
available invertebrates, especially of ants and spiders, in
June 2015 ECOLOGICAL RESTORATION33:2 175

our study area is needed to resolve this discrepancy. Collembolans and ants were the most abundant arthropods
collected in pitfall traps in mesic flatwoods of Florida
(Jennings et al. 2012). Some ant species are abundant in
disturbed areas, like the powerline corridors abutting the
introduced populations in this study (e.g., Cumberland
and Kirkman 2012). In addition, greater amounts of forest
floor leaf litter were likely present in established sites and
wolf spiders (Araneae: Lycosidae), a common prey taxon
observed in Dionaea traps, can be more abundant in forested sites compared to burned or logged sites in Florida
sand pine scrub habitat (Greenberg and McGrane 1996).
As a result, local land use, including the clearing treatment
itself, may have contributed to the difference in dominant
prey taxon. Still, reliance on several types of ubiquitous
ground-dwelling arthropods appeared to facilitate the
success of flytraps in the restored sites.
While our study examined restoration success at the level
of individual plants in multiple populations, restoration
success at the population level was not measured. A census
of the nine introduced sites six years after restoration found
populations at most sites remained intact despite being
burned by a large wildfire and altered by logging activity
associated with post-fire management (Luken 2012). Nevertheless, numbers of individual plants decreased in most
of the introduced populations (Luken 2012) demonstrating that longterm success of introduced plant populations
needs continuing attention despite monitoring of plant
reintroductions rarely lasting beyond four years (Godefroid
et al. 2011). Our study showing similar function between
introduced and established individual plants suggests
exogenous factors like anthropogenic disturbances pose
a greater threat to Venus flytrap populations.
Restoring Venus flytrap populations is most successful
when areas known to historically contain the species are
managed (Luken 2005, 2012). Growth-suppressed plants
already present benefit in these conditions, as well as propagules introduced from nearby populations. Our results
provide an additional factor, sufficient numbers of grounddwelling arthropods, for land managers who are tasked
with maintaining and restoring Venus flytrap populations
to consider. While invertebrates are seemingly ubiquitous, applications of pesticides targeting invertebrates will
reduce the prey base that provides limiting nutrients to
carnivorous plants. Such applications may occur in areas
managed for invasive insects such as fire ants, which are
frequently associated with corridors such as power lines.
Widespread applications of insecticides to forests and
wetlands for control of forest tree pests (e.g. southern
pine beetles) and mosquitos represents another common
source of arthropod mortality, which may indirectly hinder
restoration of Venus flytrap populations.

176 June 2015 ECOLOGICAL RESTORATION33:2

Acknowledgments
We thank Sunni D. Stewart and Scott G. Tomko for assisting with
field collection of traps and measuring traps in the laboratory.
Trap collection was facilitated by Jamie Dozier of the South Carolina Department of Natural Resources. Two anonymous reviewers
and the managing editor provided very helpful comments on an
earlier draft.

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John J. Hutchens, Jr. (corresponding author), Department


of Biology, Coastal Carolina University, Conway, SC, USA
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James O. Luken, Department of Biology, Coastal Carolina
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