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22001166 SOUTHEASTERN NATURALIST 1V5o(3l.) :1554,9 N–5o7. 43
Ecology and Conservation of the Endangered Legume
Crotalaria avonensis in Florida Scrub
Eric S. Menges1,*, Beatriz Pace-Aldana2, Sarah J. Haller1, and Stacy A. Smith1
Abstract - We collected data from 1998 to 2014 to describe the ecology of the highly
endangered Florida scrub plant Crotalaria avonensis (Avon Park Harebells), and herein
address several hypotheses based on what was known of its biology and the biology of
co-occurring species. This perennial herbaceous legume occurs at 3 sites and prefers
microsites with more cover by bare sand than vegetation. The population at an unprotected
site has declined in size, but dynamics have been more stable at the 2 protected sites.
Marked plants have shown high survival, slow and inconsistent growth, and occasional
plant dormancy (usually 1–2 years). Avon Park Harebells is reproductively challenged,
with very low rates of fruit set and infrequent visitation by required pollinators. The hardseeded
fruits germinated at a rate of 13–56%; the germination speed seemed to increase
after scarification, though the overall rate was less than for unscarified seeds. Unscarified
seeds remained viable in the seed bank for at least 3 years. Seedlings recruited rarely,
had moderate survival, began flowering at 4 years of age or later, and reached the size of
median adult plants in 6–8 years. Herbivores affected 7–53% of plants in a given year,
but plants showed rapid compensatory resprouting. Caging plants reduced herbivory and
increased survival, growth, and flowering. Plants resprouted after fire and mechanical
disturbance and exhibited high survival and growth, but repeated disturbances by vehicles
caused increased mortality. Avon Park Harebells remains extremely endangered due to its
limited range, small population sizes, and poor seedling recruitment. To help this species
recover, we recommend fire management, protection from herbivory, introductions and
augmentations, and further study of its pollination biology.
Introduction
Narrowly endemic species present unique challenges to conservation and management.
Many of these species have specific habitat or disturbance requirements
and occur at only a few managed sites. Management activities at these sites tend to
focus on ecosystem structural or functional properties or perhaps are aimed at restoring
populations of economic, keystone, or foundation species. Few studies have
evaluated whether broad-scale management regimes also work to benefit individual
rare species (Menges and Weekley 2013).
The Lake Wales Ridge (Weekley et al. 2008) in south-central Florida is a hotspot
for endemism. It supports one of the highest concentrations of endemic plants in
the US (Christman and Judd 1990, Dobson et al. 1997, Estill and Cruzan 2001).
Most of these species occur in xeric upland habitats, including Florida scrub and
sandhills. Over 85% of the natural vegetation on the Lake Wales Ridge has been lost
1Plant Ecology Program, Archbold Biological Station, 123 Main Drive, Venus, FL 33960.
2The Nature Conservancy, Disney Wilderness Preserve, 2700 Scrub Jay Trail, Kissimmee,
FL 34759. *Corresponding author - emenges@archbold-station.org.
Manuscript Editor: Julia Cherry
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to development (Weekley et al. 2008). Like most Florida vegetation (Slapcinsky et
al. 2010), Florida scrub and sandhill biodiversity depends on periodic fire (Menges
2007, Menges and Gordon 2010).
Among the many Lake Wales Ridge endemic species that are endangered or
threatened, Crotalaria avonensis DeLaney & Wunderlin (Avon Park Harebells)
stands out as one of the most imperiled (Turner et al. 2006). It is one of the most narrowly
distributed of all Lake Wales Ridge endemics and 1 of only 2 such species—the
other being Dicerandra christmanii Huck and Judd (Garrett’s Mint)—found at fewer
than 5 sites (Turner et al. 2006). Avon Park Harebells was listed as one of the 8 Lake
Wales Ridge species for which translocation and captive propagation may be necessary
for species survival (Turner et al. 2006). Wild populations of this federally
endangered and recently described plant are known from only 3 sites (DeLaney and
Wunderlin 1989) covering about 518 ha (USFWS 2006). Two of the sites are protected
and 1 is not. Within these sites, the distribution of Avon Park Harebells is patchy,
even within appropriate habitat (USFWS 2006). A recent 5-y review of this species
stated that it is “at grave danger of extinction” and that “without active and concerted
conservation efforts, this species may be lost” (USFWS 2006).
Recovering any species requires information on its habitat requirements, ecology,
interactions with other species, and vulnerabilities to human activities. This
information is lacking for Avon Park Harebells. Prior to our work, the only publication
regarding this plant was the species description (DeLaney and Wunderlin
1989). Here, we draw on demographic research from 1998–2014 to paint an ecological
portrait of Avon Park Harebells and suggest key issues for its conservation.
At the start of this study, little was known of the ecology of Avon Park Harebells.
Based on the biology of species with a similar life history and that occur in Florida
scrub, we suggest the following hypotheses:
• Like many diminutive Florida scrub herbaceous plants (Menges et al.
2008), Avon Park Harebells should be more likely found in open microsites.
• Unprotected Florida scrub sites are not managed using fire (Menges
1999) and have other stressors; thus, we predict that population trends
will be more positive in protected sites.
• This species has a deep taproot (DeLaney and Wunderlin 1989), so we
expect Avon Park Harebells to be long-lived, with high survival and
moderate growth.
• As a hard-seeded legume (DeLaney and Wunderlin 1989), we hypothesize
that this species has a persistent seed bank and that scarification will
increase germination speed.
• As has been reported for other large-seeded plants, we expect strong
seedling recruitment in Avon Park Harebells (Moles and Westoby 2004).
• We hypothesize that herbivory will reduce vital rates, but that recovery
from the strong taproot will allow some compensatory responses to herbivory
(paralleling responses in other Florida scrub species; Kettenring
et al. 2009, Tye et al. 2016).
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• We hypothesize that the long taproot will allow Avon Park Harebells to
readily resprout post-fire (Menges and Kohfeldt 1995).
Field-site Description
All 3 known wild populations of Avon Park Harebells occur within a small area
of northern Highlands and southern Polk counties in south-central Florida (Fig. 1).
Carter Creek, a tract of the Lake Wales Ridge Wildlife and Environmental Area
(LWRWEA) managed by Florida Fish and Wildlife Conservation Commission
(FWC), and Saddle Blanket Scrub, owned by The Nature Conservancy (TNC),
are protected. Avon Park Lakes, a sprawling subdivision, supports an unprotected
population just south of Saddle Blanket Scrub (Fig. 1). The Avon Park Lakes population
is currently at risk due to likely further residential development.
We have been studying the ecology of Avon Park Harebells since 1998, primarily
at Carter Creek. We have also periodically sampled population dynamics at the
2 other sites. All 3 sites contain a variety of plant communities, including 2 types
of Florida scrub (rosemary scrub and scrubby flatwoods) that support Avon Park
Harebells. These types of Florida scrub are well-drained shrublands dominated
by Quercus spp. (oaks), Sabal spp. (palmettos), ericads, and Ceratiola ericiodes
Michx. (Florida Rosemary). These communities are affected by periodic fire at intervals
generally ranging from 5 to 60 years (Menges 2007). We also noted plants
in a third vegetation type: sandy roadsides. We compared much of our observational
and experimental data among rosemary scrub, scrubby flatwoods, a nd roadsides.
Methods
Study species
Avon Park Harebells is a low-growing legume found in Florida scrub (rosemary
scrub, scrubby flatwoods, and roadsides) on xeric white sands (DeLaney and
Wunderlin 1989). It can be clearly distinguished from other Crotalaria species
(rattleboxes) by several flower characters (DeLaney and Wunderlin 1989). Avon
Park Harebells differs from its relative C. rotundifolia (J.F. Gmelin) (Rabbitbells)
by its curved (vs. geniculate) style, compact growth form, and pubescence.
Avon Park Harebells is deeply rooted, single to multi-stemmed, and non-clonal.
It generally flowers in the spring, is vegetative after June, and dies back over winter
(DeLaney and Wunderlin 1989). Flowers are perfect and include anthers that
release pollen at different times. Fruits are legumes containing multiple hard seeds
that are released when fruits dehisce.
Microhabitat preferences
In 2002, we collected data on microhabitat preferences by habitat for Avon Park
Harebells at both Carter Creek and Avon Park Lakes within 25-cm-radius circular
quadrats. At Carter Creek, we selected all demography quadrats (see section
on population dynamics and vital rates), most of which were occupied by Avon
Park Harebells. We also selected unoccupied quadrats at random directions and
distances (within 5 m of occupied quadrats). At Avon Park Lakes, we searched
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for occurrences of Avon Park Harebells along roadside edges and adjacent scrub.
Again, we selected unoccupied quadrats at random directions and distances from
occupied plots, but stayed within generally similar roadside habitat. In these small
circular quadrats, we recorded ocular cover-estimates (nearest 10%, plus trace
coded as 1%) on a series of microhabitat variables (percent bare sand, percent
Figure 1. Map showing locations of 3 wild Crotalaria avonensis (Avon Park Harebells)
populations on Florida’s Lake Wales Ridge (darker shading) in Polk and Highlands counties
(lighter shading).
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vegetation cover, percent litter, and percent ground lichens) and the presence of
all vascular plants and ground lichens. We used separate t-tests for roadsides and
scrub sites to compare microhabitats of occupied and unoccupied plots. We used
chi-square tests to evaluate the association of the more common species with presence
of Avon Park Harebells, separately for scrub and roadside sites.
Occupancy and densities across landscapes
We tracked Avon Park Harebells distribution and abundance across large spatial
scales at its 3 known sites. During extensive searches in the spring of 2005 (Avon
Park Lakes and Carter Creek), and 2005–2006 (Saddle Blanket Scrub), we recorded
all known spatial locations with a Trimble® handheld GPS and marked each with a
stake flag. Every 3 years thereafter (in April and May), we returned to each point at
Carter Creek and Avon Park Lakes and counted the number of Avon Park Harebells
plants within a 5-m (Avon Park Lakes) or 2-m (Carter Creek) radius of the GPS
point. At Saddle Blanket Scrub, we made counts within randomly selected 10 m x
10 m grids cells in 2009, 2010, and 2013. For all populations, we re-counted plants
in non-overlapping plots and defined a plant as all stems within 2 cm of each other.
We used t-tests to compare densities among populations.
Population dynamics and vital rates
At Carter Creek, our demography study plots were distributed throughout the
area known to support Avon Park Harebells. We set up belt transects that traversed
patches of plants in 1998, 2001, 2002, 2003, and 2005. Within each belt transect,
we chose five 25-cm circular quadrats with stratified random positions and permanently
marked them with flags and tags. Not all established quadrats supported
Avon Park Harebells. We set up a total of 105 quadrats.
Within each quadrat, we initially mapped, and later marked with plastic toothpicks
(of various colors and playing card suits) each Avon Park Harebells individual.
This species is characterized by frequent appearances and disappearances of
aboveground stems accompanied by small shifts in positions, likely reflecting its
branching root system (Delaney and Wunderlin 1989), which makes it challenging to
distinguish and follow individuals. A limited excavation at the beginning of the study
showed that the tan-colored and thickened roots were located at least 5 cm below the
soil surface and sometimes as deep as 7 cm. Relatively slender stems radiated from
root crowns through the sand at various angles. We determined that the resulting
aboveground shoots could emerge at distances of 0–10 cm from the root crown; we
used this distance range to distinguish between presumed individuals.
We conducted most of our demographic sampling during the periods of early
seasonal growth, flowering, and fruiting. We sampled quadrats monthly from February
through August in 1998–1999 and from February through June from 2000
to 2014. For each plant, we recorded survival and the numbers of stems, branch
tips, flowers (showing yellow corolla), developing fruits (green), and mature fruits
(darker). From these monthly data, we summarized annual population size and
vital rates (survival, dormancy, relative growth rates, and maximum and totals for
reproductive variables). Each year, we annually calculated relative growth rate on
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the basis of size (maximum number of branch tips in a year): positive values indicated
growth, zero indicated the same number of branches, and negative values
indicated reductions in size. We employed chi-square tests and analysis of variance
(ANOVA) to compare survival and growth, respectively, among vegetation types.
We estimated percent fruit initiation and fruit maturation by calculating the total
number of flowers, initiated fruits, and mature fruits counted in each monthly census.
These are not exact measures of fecundity because we may have missed some
reproduction between censuses or we may have double-counted some reproduction.
For mature fruits found on plants within demographic plots, we measured the
capsule length and counted the seeds per capsule in the field. We then returned them
to a an open location within the quadrat. For fruits outside the plots, we returned
them to the lab and collected data, then used the seeds in germination experiments
(see section on seed germination experiments). We characterized the distributions
of seed number per capsule and used correlations to examine the relationship between
seed number and capsule length.
Pollination biology and breeding system
In 2004, we made observations of pollinators at Carter Creek and attempted
a breeding-system study. We recorded very few flower visitors; thus, we did not
pursue analysis of these data. We were unable to conduct specific crosses in the
field because of the small size of flower parts. However, we evaluated the breeding
system of Avon Park Harebells by comparing fruit initiation from 10 plants (9 of
which opened 75 flowers) from which we excluded pollinators with mesh bags and
10 control plants (8 of which opened 66 flowers). We marked individual flowers at
1–3-d intervals with colored thread and identified each by position on the plant. We
followed subsequent fruit initiation several times per week. We defined initiation as
occurring when we observed small pods. Flowers that did not initiate fruit typically
dropped off after a few days. We analyzed the effects of the bagging treatment using
the Mann-Whitney U-test.
Seed-germination experiments
The low fecundity of Avon Park Harebells made it impossible to conduct germination
trials in most years. Here, we describe 2 experiments undertaken in 2004
and 2012.
2004 germination experiment. In spring 2004, we collected 317 seeds from Avon
Park Harebells plants at Carter Creek (outside our study plots) for use in a germination
experiment. The major factors in the experiment were scarification with
sandpaper (n = 163 vs. no scarification, n = 158) and seed color (black: n = 194, purple:
n = 65, green: n = 58). Scarification might be expected to enhance germination in
a hard-seeded legume, and it significantly increased germination in other Crotalaria
species (Wiggers 2011). We surmised that green seeds were immature (they were
rather soft) and black seeds (the hardest) were the most mature. The experiment was
initiated on 19 May 2004 within a week of seed collection. We sowed seeds in sand
and placed the flats on an open but covered veranda at Archbold Biological Station
where they were watered frequently. We monitored this experiment twice per week
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for several months, and then less frequently for 2 years. We analyzed germination using
binary logistic regression and time to germination using t-tests.
2012 shadehouse germination experiment. To test the effects of scarification on
seed germination and to gain insight into germination requirements of unscarified
Avon Park Harebells, we initiated a germination experiment in the Archbold Biological
Station shadehouse. On 9 July 2012, we scarified 70 seeds and left 70 seeds
unscarified as controls, using only mature (purple or black) seeds collected from
plants at Avon Park Lakes. We weighed the individual seeds prior to sowing. We
conducted scarification in a lab setting, using a single-blade razor to manually nick
the seed coat opposite the hilum less than 1 h before sowing. In the shadehouse, we filled
flats separated into individual cells with native soil and sowed a seed in each cell. We
randomized sowing locations and standardized sowing depth at 1 cm. We irrigated
the flats every other morning and the flats were open to rainfall. We assessed germination
daily for the first 2 weeks, every other day until March 2013, and once each week
through December 2013. We excluded all 21 seeds weighing less than 0.03 g from our
analyses because no seeds that small germinated. We used binary logistic regression
to analyze germination and a Mann-Whitney U-test to analyze time to germination.
Seedling recruitment, survival, and flowering
We assessed seedling recruitment as part of our monthly demographic sampling
at Carter Creek. From 2004 to 2011, we sampled monthly year-round in quadrats
with a history of fruit or seedling production. Following initial germination experiments
in 2004, we were able to recognize seedlings in the field because they
had glabrous, glandular cotyledons that possessed an evident midrib, were oval in
shape, and had an opposite arrangement. Subsequent true leaves were pubescent
and non-glandular. Once seedlings recruited, we followed their vital rates during
regular demographic censuses. Sample sizes were too small for statistical analyses.
Herbivory
Avon Park Harebells is commonly eaten by animals. This herbivory often involves
complete removal of stems, but sometimes just leaves and parts of stems
are affected. Herbivores include mammals, ants, and the larvae of Utetheisa
bella (L.) Pease (Bella Moth), an insect that sequesters toxins from Avon Park
Harebells tissues and uses these chemicals to deter predators (Mattocks 1986).
During each monthly demographic survey, we tracked herbivory on plants, coding
it as partial herbivory (some stems eaten, some not), total herbivory (all stems
clipped), or post-herbivory (plants recovering from total herbivory). We generally
did not record less extreme damage to portions of stems or leaves. For data analyses,
we aggregated herbivory for the entire year, with plants coded as suffering
herbivory (at least once) or no herbivory. We compared herbivory among vegetation
types using chi-square tests.
Beginning in June 2012, we experimentally caged half (n = 23) of our study
quadrats that contained living plants in 2011 or 2012. The wire cages had a mesh
size of ~1 cm, were about 50 cm in diameter, 45 cm tall, and open at the top to allow
free access to insects but deter small and large mammals. We hypothesized
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that these cages would reduce observed herbivory levels. We did not necessarily
expect an effect of caging on vital rates because observed herbivory had no obvious
effects on vital rates such as survival. We used a chi-square test to analyze
effects of caging on survival and flowering, and t-tests to evaluate caging effects
on relative growth rate.
Effects of fire and mechanical treatments
A prescribed burn took place in one of the Carter Creek study populations (the
Rosemary Path population) on 19 August 2005. This burn was primarily designed
as part of a larger project testing the effects of mechanical treatment and fire on
rosemary–oak scrub. However, we appended a small experiment to test the effects
of mechanical treatment and fire vs. fire-only on Avon Park Harebells. Before
the fire, 10 quadrats (1–10) were mechanically treated using a Gyro-Trac, a large
bulldozer-like machine that cut all vegetation near ground level and caused moderate
soil disturbance. Five additional quadrats (11–15) were burned without prior
mechanical treatment. All quadrats in both areas were thoroughly burned, although,
because fire intensity varied, we noted quadrats as being lightly or intensely burned
within a month of fire. We checked the response of Avon Park Harebells plants
monthly, assessing survival, size, flowering, and recruitment. We analyzed treatment
effects on survival with chi-square and on relative growth rate (based on
number of branch tips) using one-way ANOVA.
Effects of vehicles
Repeated damage from vehicles at Carter Creek provided an opportunity to examine
the resilience of Avon Park Harebells to different types of damage. Before
2008, the Carter Creek site was unfenced and subject to a great deal of all-terrain
vehicle (ATV) traffic. Quadrats in 1 subpopulation were run over repeatedly in
2004, 2005, and 2006. Nearly all existing plants appeared to have been killed. Each
year, we found the quadrats and followed the recovery of the population. During
2008, the FWC completed fencing the Carter Creek site so that damage from ATVs
and truck traffic would no longer af fect the population.
Other quadrats (16–25) with Avon Park Harebells plants were inadvertently
damaged in 2007 and/or 2009 during pre-burn site preparation by a Gyro-Trac. The
Gyro-Trac crushed plants, rather than uprooting them, as often occurs with ATV
and truck traffic. The 2009 gyrotracking was followed with a prescribed burn that
also included vehicle damage to Avon Park Harebells quadrats. Sample sizes affected
by vehicles were too small for statistical analyses.
Results
Microhabitat preferences
Within Florida scrub, Avon Park Harebells prefers sites with more bare sand than
vegetation cover (Table 1). Similarly, in scrub locations, the species was positively
associated with an open-site herb, Cnidoscolus urens var. stimulosus (Finger Rot),
and negatively associated with a dominant shrub, Quercus inopina (Sandhill Oak)
(Table 2). On disturbed roadsides, Avon Park Harebells occurred in microhabitats
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that were not different than random locations, and all tested species associations
along roadsides were not statistically significant (Table 2).
Occupancy and densities across landscapes
Occupancy percentages of Avon Park Harebells have declined in all populations
over the years (Fig. 2). Initial occupancies in 2005 or 2006 were, by definition,
100% because we set up all points at Avon Park Lakes, Saddle Blanket Scrub, and
Carter Creek in patches of plants. Avon Park Lakes had a strong decline in occupancy
between 2005 and 2008, and a slow decline since then. The 2 managed sites,
Table 1. Microhabitat differences between locations occupied by Avon Park Harebells (occ.) and random
locations (not occ.) in Florida scrub and roadside habitats at 2 sites (Carter Creek and Avon Park
Lakes). Percent bare sand was strongly negatively correlated with % litter; thus, we did not include
the latter. Significance (Sig.) was corrected for tests of 3 variables. NS = P > 0.05.
Scrub (Carter Creek only) n = 94 Roadside (2 sites) n = 92
Mean Mean P Mean Mean P
Measure occ. not occ. t uncorrected Sig. occ. not occ. t uncorrected Sig.
% vegetation cover 24.0 56.1 6.8 less than 0.001 less than 0.001 23.0 28.6 1.3 0.245 NS
% lichen 10.0 12.4 0.9 0.383 NS 15.5 24.8 2.2 0.032 NS
% bare sand 44.0 12.0 6.3 less than 0.001 less than 0.001 45.7 34.0 1.8 0.075 NS
Table 2. Percent occupancy for the 12 most-common species in microhabitat plots in the area of Avon
Park Harebells populations at Carter Creek and Avon Park Lakes, presented by habitat (Florida scrub
or roadside) and whether microhabitat plot was occupied or unoccupied by Avon Park Harebells. P
values are shown for chi-square tests for difference between unoccupied or occupied plots within each
habitat. In each case, n = 94, df = 1. NT = no test performed due to ≥2 cells with an expected count
less than 1. * indicates signicifance (P < 0.05). % U = % in unoccupied plots; % O = % in occupied plots.
% of Florida scrub plots Roadside plots
Species plots % U % O P % U % O P
Cladonia leporine Fr. (Cup Lichen) 38 21 33 0.196 49 49 0.974
Cladonia subtenuis (Abbayes) Mattick 36 44 48 0.692 30 20 0.296
(Reindeer Lichen)
Aristida spp. (three-awn grasses) 26 10 15 0.486 42 38 0.768
Polygonella myriophylla (Small) Horton 25 19 24 0.541 28 28 0.992
(Small’s Jointweed)
Selaginella arenicola Underw. (Sand 23 12 9 0.550 36 33 0.802
Spikemoss)
Quercus inopina Ashe (Sandhill Oak) 22 50 28 0.031* 4 5 NT
Licania michauxii Prance (Gopher Apple) 14 19 20 0.920 9 8 NT
Serenoa repens (W. Bartram) Small 14 23 22 0.891 6 5 NT6
(Saw Palmetto)
Cladonia evansii Abbayes (Powder-puff 13 27 21 0.547 2 0 NT
Lichen)
Stipulicida setacea Michx. (Pineland 11 6 17 0.093 11 8 0.563
Scaleypink)
Cnidoscolus urens (L.) Arthur var. 9 2 20 0.006* 9 3 NT
stimulosus (Michx.) Govarts (Finger Rot)
Quercus geminata Small (Sand Live-oak) 8 6 13 NT 6 5 NT
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Saddle Blanket Scrub and Carter Creek, have had a consistently slow rate of decline
in percent occupancy. This overall decline has occurred despite the fact that about
15% of all occupied plots that became unoccupied became occupied once again in
subsequent samples.
In contrast, the number of plants per occupied plot has not generally shown consistent
patterns (Table 3). Mean and median numbers of plants have been consistent
at Avon Park Lakes despite the loss in occupied plots, but have increased at Saddle
Blanket between 2009 and 2010 and changed little from 2010 to 2013. At Carter
Creek, there was a substantial increase in the mean but not the median between
2009 and 2012 (Table 3). Plant densities were significantly higher at Carter Creek
(median ± SE = 1.42 plants/m2, ± 0.32, P < 0.05) than either Avon Park Lakes (0.12,
± 0.02) or Saddle Blanket Scrub (0.10, ± 0.02); the latter 2 sites had statistically
similar densities.
Population dynamics
Avon Park Harebells populations at Carter Creek tended to have slow declines
from 1998–2009, but have remained fairly stable or increased from 2009 to 2014
Figure 2. Percent occupancy of Avon Park Harebells at 1 unprotected site (Avon Park
Lakes) and 2 protected sites (Saddle Blanket Scrub and Carter Creek) from 2005 to 2014.
By definition, all studies started with 100% occupancy because points were located at all
known patches of plants. The Saddle Blanket Scrub initial survey occurred over 2 years
(2005–2006).
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(Fig. 3). Within years, plant numbers generally increased from February through
April or May, although patterns varied annually.
Vital rates
Annual survival. Median annual survival for Avon Park Harebells has been consistently
high. Including plant dormancy, annual survival has been about 86%, with
Table 3. Mean, standard error, and median number of Avon Park Harebells plants per occupied plot
at Avon Park Lakes, Saddle Blanket Scrub, and Carter Creek. Plots are in a 5-m-radius circle at Avon
Park Lakes, 10 m x 10 m square at Saddle Blanket Scrub, and 2-m-radius circle at Carter Creek. Mean
densities per m2 are also shown. These data were not collected for the initial years of the study (2005,
2006) when plots were set up and occupancy was recorded.
Population Year Mean # SE Median # Mean density
Avon Park Lakes 2008 17.0 3.0 11 0.22
2011 19.1 2.9 11 0.24
2014 19.2 4.7 10 0.24
Saddle Blanket 2009 9.8 1.3 5 0.10
2010 14.9 1.8 9 0.15
2013 15.2 1.8 9 0.15
Carter Creek 2009 15.8 4.1 6 1.25
2012 24.2 7.1 6 1.92
Figure 3. Population trends in Avon Park Harebells study plots at Carter Creek during
monthly monitoring February through June from 1998 to 2015. Each line shows the number
of plants for the set of plots initiated in the year shown. The x-axis labels indicate the start
of each sample year.
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little variation (range = 82–92%; Fig. 4). Annual survival varied among vegetation
types (rosemary scrub, scrubby flatwoods, and roadsides) in 6 of 16 years (Fig. 5).
In 5 of 6 cases in which annual survival differed significantly, plants in rosemary
scrub had higher survival. In early years, roadside plants often had the lowest
survival, likely due to vehicle damage.
Dormancy. Both within-year and full-year plant dormancy are characteristic of
Avon Park Harebells. Based on data from 1999–2013 (dormancy cannot be calculated
directly from the first and last years of our longitudinal data), about 12% of
plants (95 of 802) in our dataset had at least a full year of dormancy, and the median
annual dormancy was 7% of living plants (Fig. 4). Just over half of plants recorded
as dormant at some point during our study were dormant for only 1 years (54%), but
we recorded 1 case each of plants that were dormant for 7 and 8 years. The mean
length of dormancy for plants with at least 1 years of dormancy was 1.99 years.
Only 8 plants were dormant twice, and 1 plant was dormant 3 times.
Growth. Avon Park Harebells plants do not show consistent positive growth
(increase in size from year to year). On average, growth was slightly negative and
more plants regressed (42%) than grew (38%) (Table 4). These patterns varied year
to year. In 2 years, half or more plants became smaller, and in 3 years, half or more
plants grew larger. A consistent proportion (14–24% by year) maintained the same
number of branches. Vegetation type had an effect on growth in only 5 years (of
Figure 4. Total percent of Avon Park Harebells plants surviving (including dormant), surviving
aboveground, and surviving plants that were dormant annually from 1998–1999 through
2013–2014 at Carter Creek. Year on X axis refers to second year of annual survival (e.g.,
2004 indicates survival from 2003–2004).
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16 y), with plants in scrubby flatwoods showing lower growth than plants along
roadsides or in rosemary scrub (Table 4).
Flowering and fruiting. Avon Park Harebells at Carter Creek are reproductively
challenged. Flowering peaked in April in 10 of 14 years since 2000, and fruits were
most abundant in May or June. Nonetheless, few fruits were produced. Fruits were
initiated from less than ¼ of flowers in most years, and maturation rates were often less than 5%
(Fig. 6). Low fecundity in Avon Park Harebells is clearly one of the factors contributing
to poor recruitment.
Slightly more than half of Avon Park Harebells plants had consistent flowering
status from year to year. For example, 61% of plants that were vegetative in 2012
remained so in 2013 and 2014, while the remaining plants flowered once or twice.
Fifty-three percent of plants that flowered in 2012 flowered in all 3 years, but the
remainder reverted to being vegetative for 1–2 years. However, between 2012 and
2014, 41% of all plants switched between vegetative or flowering .
Fruit lengths were slightly right-skewed from normal, with a range of 1.7–3.1
cm), a mode of 2.7 cm, and a mean and median of 2.5 cm. Seed number also
Figure 5. Annual survival aboveground for Avon Park Harebells plants by vegetation type
at Carter Creek. Year refers to the second year of the annual sequence (e.g., 2005 refers to
2004–2005 annual survival). Plants moving into or out of dormancy are not included. Bars
are shown in cases with n > 9 plants.
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exhibited a range of 4–18 seeds per fruit (mean = 9.3, median = 8, mode = 7) and
were slightly left-skewed. The number of seeds was not significantly correlated
with capsule length (r = 0.151, n = 56, P = 0.262).
Pollination biology and breeding system
In 2003, we observed a diversity of floral visitors (mainly bees) on Avon Park
Harebells, although insect visits were quite infrequent. Flowers seemed to open
about 10:00 AM and were produced on the same plant for many weeks. Flowers
were protandrous. Casual observations in subsequent years confirmed that insect
visitation was quite rare.
None of the 75 flowers from which we excluded pollinators initiated fruits
(0 fruits on 9 plants). We observed low rates of fruit initiation on control plants—8
fruits developed from 66 flowers (12.1%) on 3 of the 8 plants that flowered.
Although this is a small experiment and only 3 of 17 plants initiated fruits, the treatment
difference was nearly significant (Mann-Whitney U = 22.5, P = 0.051). Fruit
production among plants was highly variable, a pattern that also occurred in plants
followed in our demography quadrats.
Table 4. Growth statistics for Avon Park Harebells. For each year, the number of plants and the mean
and standard deviation of annual relative growth rate (RGR), based on number of branches, is shown.
We also show percent of plants regressing, growing, or remaining with the same number of branches,
as well as the effects of vegetation type on growth in 1-way ANOVAs. In years when some plants
were caged, we conducted separate analyses for caged and uncaged plants and overall. * indicates ≥1/2
of the plants were either regressing or growing in size. Vegetation types: RS = rosemary scrub, SF =
scrubby flatwoods, Road = roadsides.
Annual RGR Percent of plants Veg. type Greatest
Years n Mean SD Regressing Same Growing effect (P) growth
1998–99 101 -0.49 0.74 69 14 17 0.221 -
1999–00 103 -0.05 0.77 41 19 40 0.409 -
2000–01 91 0.21 0.69 29 21 50 0.002 RS
2001–02 162 0.16 0.70 30 23 47 0.035 Road
2002–03 211 -0.18 0.72 49 22 29 0.726 -
2003–04 229 0.09 0.65 33 17 50 0.380 -
2004-05 217 -0.09 0.65 48 21 31 0.003 Road
2005–06 227 -0.18 0.71 48 16 35 0.026 RS
2006–07 221 0.15 0.80 37 12 51 0.000 Road
2007–08 212 -0.08 0.60 50 18 32 0.353 -
2008–09 202 0.04 0.69 43 13 44 0.934 -
2009–10 197 0.02 0.63 36 23 41 0.068 -
2010–11 185 -0.07 0.69 45 17 38 0.051 -
2011–12 182 -0.14 0.69 46 24 30 0.433 -
2012–13 191 0.20 0.69 29 20 51 0.855 -
2012–13 Caged 97 0.32 0.77 27 14 59 0.884
2012–13 Uncaged 94 0.09 0.58 31 26 43 0.945
2013–14 201 -0.17 0.69 44 26 30 0.750 -
2013–14 Caged 107 -0.06 0.64 36 31 33 0.835
2013–14 Uncaged 94 -0.29 0.63 53 20 27 0.520
Mean 183 -0.04 0.69 42 19 38 - -
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Seed germination
2004 germination experiment. Germination began in the first few weeks of the
study, with 37 seeds (11.3%) germinating in the first month. Three more seeds
(0.9%) germinated in the first summer, and 3 seeds germinated in the second year
of the experiment. These results demonstrated that Avon Park Harebells has a persistent
seed bank, although germination rates after 1 year were below 1%.
The overall germination rate through May 2007 was 13.2%. Germination
percentages were much lower for green seeds (1.7%) than for purple (12.3%) or
black (17.0%) seeds. Scarification reduced germination percentages (10.1% vs.
16.5%) and eliminated germination of green seeds. Seed color, but not scarification,
was a significant predictor of germination in binary logistic regression
(log likelihood = 124.2, df = 2, P < 0.001). When we removed green seeds from
the analysis, neither the color of the seeds (purple vs. black) nor the scarification
treatment affected germination (binary logistic regression, P > 0.15 for
each variable). For black seeds alone, scarification did not affect germination
percentage. Scarified seeds germinated marginally more quickly than non-scarified
seeds (t = 2.04, df = 26, P = 0.052) in a mean time of 0.25 months vs. 2.5
months for non-scarified seeds. The effect of scarification on germination time
was somewhat more pronounced for black seeds (t = 2.19, df = 16, P = 0.044);
purple seeds only germinated in the first month. All scarified seeds germinated
Figure 6. Estimated percentage of Avon Park Harebells flowers initiating or maturing fruits
during the period 2000–2014 at Carter Creek, inferred from monthly counts of flowers,
initiated fruits, and mature fruits.
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within 2 months, while non-scarified seeds germinated in both the first 2 months
(23 seeds) and in the second year (3 seeds).
2012 shadehouse germination-experiment. For seeds heavy enough (>0.03
g) to germinate (no seeds less than 0.03 g ever germinated), germination percentages
through December 2013 (17 mo) were high (56.3%). Over 70% of the
germinants had emerged within 3 months during the summer of 2012 (Fig. 7).
However, germination beyond 12 months (about 6% of germinants) again confirmed
that Avon Park Harebells can persist in the seed bank. Both scarification
treatment (B = 4.00, Wald = 6.09, df = 1, P = 0.014) and seed dry-weight (B =
370.1, Wald = 4.77, df = 1, P = 0.029) but not their interaction (B = -346.6,
Wald = 2.02, df = 1, P = 0.155) predicted whether seeds germinated. Germination
percentages were much higher for non-scarified seeds (77%) than scarified
seeds (36%) during this 17-mo experiment. Heavier seeds were more likely to
germinate than lighter seeds.
Scarification affected time to germination (Fig. 7); scarified seeds germinated
significantly faster post-sowing than non-scarified seeds (median days
to germination = 9 vs. 58; Mann-Whitney U = 16.0, P ≤ 0.001). Non-scarified
seeds continued to germinate throughout the experiment and during most
months of the year.
Figure 7. Number of Avon Park Harebells germinants by week after sowing for scarified
and nonscarified seeds in the 2012 Archbold Biological Station shadehouse experiment. No
seeds germinated during the final 8 weeks of the experiment (wee ks 63–71).
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Seedling recruitment, survival, and flowering
We observed seedlings recruiting sporadically and in most years from 2004–
2010 (Table 5). Less-frequent sampling after 2010 probably explains part of the
drop in seedling numbers in the most recent years. Seedlings recruited throughout
the year, but mostly appeared during late spring and summer.
Seedlings survived well but grew slowly. Seven of the 32 seedlings found
since 2004 were still alive through 2014 (Table 5). Seedling survival was moderate
after the first year, but then rose to >80% from the second year onward
(Fig. 8). However, seedlings had variable and often fairly slow growth. Mean
number of branches by age increased from 1.5 in the first year to 2.6 by the third
year, and to 6.0 by the eighth year. Although sample sizes are small, 6–8-year-old
seedlings had similar mean and median numbers of branches as the overall population
(5.5 and 3, respectively).
Avon Park Harebells does not become reproductively mature for several years.
Over the years, we have noted flowering in 4 plants first observed as seedlings. The
age of first flowering has varied from 4 to 7 years (Table 5), with a median age at
first flowering of 5 years. One seedling flowered twice and 1 seedling flowered 3
times. However, 3 plants surviving to 2014 never flowered, despite surviving for
6–9 years. The percent of plants flowering increased slowly from age 4 through
ages 6–8, although less than 1/3 of the oldest seedlings flowered in any given year (Fig. 8).
Herbivory
Herbivory is a common but variable event for Avon Park Harebells. About 16%
of our study plants had evidence of herbivory in any given year (Table 6); this rate
varied widely from 7% to 53% from 1998 to 2014. The 2 years with the most herbivory
were 2008 and 2009. We believe that the high level of herbivory in 2009 was
mainly due to Bella Moth larvae because we observed many caterpillars. Herbivory
Table 5. Summary of Avon Park Harebells seedling recruitment in the Carter Creek population since
2004. Seedlings were marked in their recruitment year and subsequently followed monthly through
June 2011, and from February through June each year since then. Ages of flowering = seedling recruitment
year defined as age zero, NA = not applicable (no plants survived to flowering), and V =
still vegetative.
Year of seeding # of seedlings Maximum # of Ages when
emergence # of seedlings alive in 2014 branches in 2014 flowering (y)
2004 2 0 - -
2005 0 0 - NA
2006 8 3 8, 9, 1 4, 7, V
2007 2 1 2 V
2008 2 1 5 V
2009 14 2 4, 6 4, V
2010 2 0 - NA
2011 0 - - -
2012 2 0 - NA
2013 0 - - -
2014 0 - - -
All cohorts 32 7 1–9 4–7
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did not consistently vary among the 3 vegetation types (Table 6). Prior to caging,
herbivory was highest in rosemary-scrub habitats from 1998 to 2000, scrubby flatwoods
from 2008 to 2010, and roadside plants from 2008 onward.
Caging, begun in 2012, significantly reduced herbivory in both subsequent years
(Table 6). Caged plants had 8% herbivory in 2014, which was significantly lower
than the 44% herbivory in uncaged plants (χ2 = 42.7, df = 1, P < 0.001). The difference
was also significant in 2013 (the first year of caging), when caged plants had
only 4% herbivory (vs. 21% in uncaged plants; χ2 = 13.3, df = 1, P < 0.001). These
observed effects of caging might be underestimates because the percentages only
include plants that emerged and were observed during monthly surveys. If plants
emerged and then were immediately eaten (or died back from drought or other
causes), we might not have recorded them in our monthly surveys.
Caging significantly increased annual survival from 2013 to 2014 (χ 2 = 9.5, df =
1, P = 0.002). Caged plants had 93% survival vs. 79% survival for uncaged plants.
Caged plants had slightly higher annual 2012–2013 survival than uncaged plants
(89 vs. 85%), but the difference was not significant (χ2 = 0.59, df = 1, P = 0.44).
However, the cages were not installed until halfway through the 2012 calendar year.
The significant cage effect on survival and the lack of prior observed herbivory effects
on survival (Menges et al. 2013) suggest that monthly censuses do not capture
all herbivory events.
Figure 8. Percent of known Avon Park Harebells seedlings surviving or flowering annually
at Carter Creek, as a function of age, determined by following naturally recruiting seedlings
over time. Plants 6–8 y old are binned under “6”. Sample sizes are n > 9 for each point.
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Caging also had positive effects on relative growth rate (based on branch
numbers) from 2012 to 2013 and 2013 to 2014 (Table 4). For 2012–2013, caging
increased growth (0.32 vs. 0.08, t = 2.31, P = 0.022). From 2013 to 2014, caged
plants had less-negative relative growth rates (-0.06) than uncaged plants (-0.29);
this difference was significant (t = 2.41, P = 0.017).
Caging also affected flowering in both 2013 and 2014. Caging had a significant
effect on flowering in 2013 (χ2 = 8.7, df = 1, P = 0.003); caged plants were more
likely to flower than uncaged plants (41% vs. 24%). In 2014, caged plants flowered
36% of the time, in contrast to uncaged plants, which flowered 20% of the time; the
difference was again significant (χ2 = 7.8, df = 1, P = 0.005).
Effects of fire and mechanical treatments
Fire and mechanical treatments had no discernable negative effects on Avon
Park Harebells. Plants rapidly resprouted (typically between 2–4 months) after
the August 2005 disturbances (fire, Gyro-Trac followed by fire). Fire had neither a
negative nor a positive effect on initial survival of Avon Park Harebells. Between
2005 and 2006, survival did not differ significantly among the various treatments
(χ2 = 3.3, df = 2, P = 0.195). Survival was similar in the burn-only quadrats (95.6%),
the Gyro-Trac + burn (87.5%), and unburned rosemary-scrub quadrats elsewhere
at Carter Creek (matching the vegetation type of the burned quadrats; 80.6%).
However, in the second year (2006–2007), survival was highest in burned quadrats
(95.6%), lowest in control quadrats (71.4%), and intermediate in combination
Table 6. Percent of Avon Park Harebells plants at Carter Creek with herbivory at some point in the
year, and effects of vegetation, by year. When vegetation effects were significant, the vegetation type
with the highest herbivory is indicated by +. x = P < 0.1, *P < 0.05; **P < 0.01; ***P < 0.001, and NS
= not significant.
Year Overall Rosemary scrub Scrubby flatwoods Roadside P
1998 9.0 17.1+ 2.7 3.4 ***
1999 11.5 24.0+ 3.4 0.9 ***
2000 9.1 18.7+ 1.3 2.6 ***
2001 10.3 9.8 12.1 8.6 NS
2002 12.5 7.8 18.8+ 12.1 **
2003 11.6 11.0 13.4 10.3 NS
2004 15.9 19.2 14.1 12.9 NS
2005 17.6 22.4+ 13.4 13.8 *
2006 6.9 3.2 14.7+ 1.8 **
2007 10.8 11.1 14.4 5.0 NS
2008 30.1 19.8 25.9 51.6+ ***
2009 52.8 75.0+ 30.3 43.8 ***
2010 24.6 16.2 44.8+ 20.9 ***
2011 20.2 8.8 18.9 41.9+ ***
2012 16.1 11.3 13.8 26.2+ *
2013 all plants 12.9 9.5 4.0 23.5+ **
2013 uncaged 21.4 16.4 7.7 32.6 x
2014 all plants 27.0 31.3+ 3.8 25.8 *
2014 uncaged 44.4 56.3+ 7.1 36.6 **
Median (uncaged) 16.1 16.2 13.8 12.9 -
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quadrats (80.9%); the difference was significant (χ2 = 6.1, df = 2, P = 0.047). Subsequently,
survival was greater in each of the treated areas (100% in 2007–2008) than
in the control (70.2%; χ2= 21.2, df= 2, P < 0.001). Beyond 2008, the advantages of
the disturbances were inconsistent.
Growth was affected by management treatments (fire, Gyro-Trac followed by
fire) for 2 of the years following management. The combination of Gyro-Trac
and fire produced higher initial growth relative to the burn only and the control
(Table 7). Two years after treatments, there was usually little difference among
treatments, although plants in the area that was Gyro-Trac–chopped and then intensely
burned sometimes had lower growth.
Effect of vehicles
Repeated, but not single, vehicle disturbances caused marked mortality of Avon
Park Harebells. At the Carter Creek plots that were run over repeatedly by ATVs
between 2004 and 2006, only 4 plants (15%) recovered, despite the removal of
traffic due to fencing in 2008. Burial of plot markers indicated that some of the
disturbances may have involved vehicles that dug well into the sandy soil. In contrast,
plants crushed by a single Gyro-Trac event during preparation for prescribed
burns survived more frequently. Nine of 19 plants (47%) crushed in 2007 and 7 of
11 plants crushed in 2009 recovered (some recovery was delayed until 2010). Plants
affected in both years rarely survived (2 of 19 marked plants). Our analysis may
underestimate the resilience of this species because their positions may have shifted
due to the mechanical disturbance and new plants later recruited into these areas.
Discussion
Support for hypotheses
Most of our hypotheses addressing the ecology of Avon Park Harebells were
supported by our long-term study. Supported hypotheses included the plant’s
preference for open microsites, more-positive population trends in protected sites,
Table 7. Effect of management treatments (burn only, Gyro-Trac [G] followed by light or intense fire)
made in August 2005 on subsequent relative growth rate (based on number of branch tips). For the
comparison, we only considered unburned rosemary-scrub sites with the same vegetation as occurred
in the area of the burn and Gyro-Trac treatments. * indicates relatively high growth in years with
significant (P < 0.05) treatment effects.
Year Unburned Burn only G + light burn G + intense burn F P
2005–2006 -0.38 0.08 0.23* 0.14* 7.6 0.000
2006–2007 -0.09 0.44 0.57* 0.73* 4.7 0.005
2007–2008 0.11 -0.09 -0.04 -0.03 1.1 0.335
2008–2009 0.21 -0.16 0.00 -0.06 1.5 0.214
2009–2010 -0.27 0.11* 0.14* -0.33 3.4 0.021
2010–2011 0.20 0.10 0.14 -0.33 1.6 0.199
2011–2012 0.19* -0.32 -0.23 -0.56 4.1 0.008
2012–2013 0.15 0.17 0.25 0.11 0.2 0.874
2013–2014 -0.07 0.06 -0.28 -0.31 1.8 0.158
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high annual survival, a persistent seed bank, increase in germination speed with
scarification, negative effects of herbivory, and post-fire resprouting. However, in
contrast to our hypotheses, Avon Park Harebells had minimal growth from year to
year and had limited seedling recruitment.
Life history and demography of Avon Park Harebells
Avon Park Harebells is a long-lived perennial herb with fairly high (about 85%)
and consistent annual survival, but inconsistent and often non-directional growth
trajectories. Seedling survival is >80% after the first year, seedlings grow slowly,
and flower between 4 and 7 years of age. Seed production and seedling recruitment
are both fairly limited. This species also is a strong resprouter after fire, herbivory,
and mechanical disturbances that remove its aboveground parts. All these traits
are typical of organisms on the slow end of the fast–slow continuum (Franco and
Silvertown 1996, Jones et al. 2008).
As a low-growing herbaceous plant growing in a shrubland (Florida scrub),
Avon Park Harebells is potentially vulnerable to aboveground and belowground
competition from the shrubs (oaks, palmettos, ericads) that dominate its habitat
(Abrahamson 1985). Little is known of rooting patterns of Florida scrub plants,
although some shrubs are deeply rooted with high aboveground:belowground
ratios (Saha et al. 2010). Avon Park Harebells is also deeply rooted (DeLaney
and Wunderlin 1989), but, aboveground, it can be easily overtopped by shrubs.
Although plants in this study showed a preference for open microsites, the species
is capable of growing beneath a shrub canopy. This characteristic contrasts with
many Florida scrub herbs that strongly specialize in gaps (Dee and Menges 2014;
Menges et al. 1999, 2008). Other herbs that are able to grow well in shrub matrices
include Liatris ohlingerae (S.F. Blake) B.L. Rob. (Scrub Blazing-star) (Petru
and Menges 2003) and Asclepias curtissii (A.Gray) (Curtiss’ Milkweed) (Mondo
et al. 2010).
Many long-lived herbaceous plants exhibit plant dormancy (vegetative dormancy,
prolonged dormancy; Shefferson 2009), during which plants spend an entire
growing season belowground. This habit may reflect an adaptive bet-hedging trait
to counter the effects of environmental stress and stochasticity (Shefferson et al.
2012). Dormancy may also be effective because plants can obtain carbon without
having aboveground parts (Shefferson 2009) or remobilize structural carbon for
subsequent re-growth (Gremer et al. 2010). Avon Park Harebells can be dormant
for an entire growing season or longer, but fewer than 10% of plants exhibit this
plant dormancy and most are only dormant for 1 year. In contrast, some orchid
populations have as many as 30% of plants dormant with many plants dormant for
multiple years (e.g., Hutchings 2010). Species exhibiting dormancy tend to grow on
dry sites, with high-light levels and infertile soil (Reintal et al. 2011); these traits
also characterize Avon Park Harebells.
Reproductive biology
Avon Park Harebells is reproductively challenged. This non-clonal species
produces limited numbers of fruits and seeds, at least at our demographic study
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site (Carter Creek). At our site, flowers were consistently produced over a period
of months, but few fruits were initiated and matured. Our breeding-system experiments
demonstrated that no fruit production occured in flowers denied access to
pollinators. This failure of bagged flowers to set fruit could be due to genetic selfincompatibility
or to the need for insect vectors to transfer self or outcross pollen.
Fruit production in unbagged, open-pollinated flowers could have resulted from
pollen movement among plants (outcrosses), between flowers of the same plant
(geitonogamy), or from insect-vectored transfer of pollen within a flower (facilitated
autogamy). Although our observations suggest that fruit set requires insect
pollinators, they do not indicate whether or not Avon Park Harebells is genetically
self-compatible. Pollinator visits to Avon Park Harebells plants appear rare, although
its pollination biology remains largely unstudied.
Seeds mature inside capsules and turn color from green to purple/brown and
black. Ripe pods dehisce and drop black seeds to the ground. Green seeds are generally
not viable, and germination of purple/brown seeds is limited to a few months
after sowing. In contrast, the mature, hard, black seeds can germinate immediately
or stay dormant for at least 2 y.
Results from our 2 shadehouse experiments showed the strong effects of
scarification in breaking seed dormancy and facilitating rapid germination. However,
germination percentages were lower with scarification, in part because only
non-scarified seeds germinated in the second year after seed production. Both
germination experiments showed peaks in germination during the first few months
after seed maturation (in the summer). Our results also showed a small, persistent
seed bank with germination in the summer of the second year. These trends are
consistent with a field germination experiment started as part of an experimental
introduction in 2012 (Smith and Menges 2013). Mechanisms for scarification in
the field probably include sand movement and heat from fires. Fire breaks physical
dormancy in species of many families (Baskin and Baskin 1998), and fire promotes
germination of buried seeds in other legumes (Bell et al. 1993, Bradstock and Auld
1995). Promotion of germination by fire-induced scarification may allow seedlings
a greater chance of survival and growth. Likewise, breakdown of the hard seed coat
over time by rain may help synchronize most germination to occur during the wetter
summer months.
Herbivory
Avon Park Harebells is affected by both mammalian and insect herbivory. One
insect herbivore is the Bella Moth larva, which specializes on Crotalaria species and
utilizes pyrrolizidine alkaloids obtained from the plants for its defense (Mattocks
1986). Damage due to insects appears variable in space and time. In some years,
damage from the Bella Moth was greater in spring vs. winter months (O’Chaney
2007). Population densities of the Bella Moth have been inflated by the spread of
exotic (African) species of Crotalaria (Mark Deyrup, Archbold Biological Station,
Venus, FL, pers. comm.). The caterpillar feeds preferentially on Crotalaria fruits,
although it selects leaves if no fruits are in the vicinity. Based on the feeding rate
of a captive caterpillar, each one is capable of completely eating an Avon Park
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Harebells fruit in a day. However, herbivory by Bella Moth appears episodic. Avon
Park Harebells are also damaged by beetles and caterpillars (O’Chaney 2007).
Herbivory of entire stems is very common. We attribute this herbivory to mammals
such as Sylvilagus floridanus (J.A. Allen) (Eastern Cottontail) or Odocoileus
virginianus (Zimmermann) (White-tailed Deer). Caging plots reduced observed
herbivory by 5-fold, and plants protected by cages had higher survival, growth, and
flowering in subsequent years. This result was unexpected, because we frequently
observed strong resprouting of Avon Park Harebells after complete herbivory, and
because observed vital rates were not related to whether we had observed herbivory
in the previous year.
Disturbance ecology
Avon Park Harebells is found only in Florida scrub, which is a pyrogenic ecosystem.
The natural fire regime for Florida scrub is characterized by infrequent,
patchy, intense fires ignited largely in the late spring and early summer (Menges
2007). Avon Park Harebells individuals and populations are resilient to fire. Plants
resprout quickly after fires, and populations do not show markedly altered survival,
growth, or fecundity. In fact, some measures of survival and growth were higher
for burned than unburned plots perhaps due to reduced competition or increased
nutrient availability post-fire.
This species is also resilient to some human-caused disturbance events, although
either frequent or severe disturbances can impact populations. Multiple disturbances
by vehicles (often within the same year), especially causing soil disturbances,
reduced populations several times during this study. Land-management practices
that merely mow or crush plants are less damaging than vehicle disturbances that
churn up the sandy soil, but even these kinds of impacts caused population declines
when they occurred only 2 years apart.
Population trends
In protected areas such as our study site (Carter Creek), Avon Park Harebells
populations appear fairly stable. Densities in our study plots have showed stability
or a slow decline over the years. Broader surveys at both protected sites have
also shown stable populations. In contrast, the single unprotected site (Avon Park
Lakes) showed a drastic decline in geographic extent (as measured by occupancy)
during a time when housing activity was high. During the recent economic recession,
new housing construction ceased and the population stabilized. However, at
this site, nearly all plants grow on roadsides and not in the very dense, overgrown,
long-unburned scrub. We have initiated an introduction of Avon Park Harebells to
a protected site using seeds and plant material from Avon Park Lakes. The introduction
is less than 3 years old, but to date has been successful (E. Menges, pers.
observ.; Smith and Menges 2013).
Conservation and management recommendations
Wild populations of Avon Park Harebells have been documented at only 2
protected sites; thus, active conservation and land management is essential to its
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E.S. Menges, B. Pace-Aldana, S.J. Haller, and S.A. Smith
2016 Vol. 15, No. 3
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persistence (Turner et al. 2006). Based on our research findings, we recommend the
following:
• Continue managing the Florida scrub sites with prescribed fire. Avon
Park Harebells responds well to fires, and fires will limit the development
of vegetation structure (tall shrubs and trees) that may harm this species
in the long run. Fire management is consistent with many conservation
objectives in Florida ecosystems (Slapcinsky et al. 2010).
• Consider additional introductions and augmentations of Avon Park Harebells
to the protected sites within its limited range. This action will provide
a bit of conservation bet-hedging against catastrophes at its current
sites and provide useful information on its management.
• Where feasible in small populations, take measures to reduce herbivory.
Caging of plants has been very successful in reducing herbivory and
increasing vital rates, and we routinely cage any introduced plants to
limit damage. Actions to control likely herbivores will be difficult to accomplish,
given the degree of suburban development within the range of
Avon Park Harebells.
• Use management that encourages pollinators (e.g., prescribed fire, avoidance
of herbicides) and consider further studies on the identities and roles
of pollinators on fecundity of Avon Park Harebells.
Acknowledgments
We thank Viani Menges, Carl Weekley, Amanda Brothers, Marcia Rickey, Christine
Bertz, Evan Batzer, Sadie Watts, Austin Ritenour, Stephanie Koontz, Kelly Peterson,
John Benning, Ryan Cressey, Britta Countryman, Devon Picklum, and Jamie Peeler for
assistance in the field. Amanda Brothers conducted the pollination and breeding systems
experiment. We are grateful to the co-operating agencies and landowners: Nicole Ranalli
and Wade Ulrey (Florida Fish and Wildlife Conservation Commission), and Steve Morrison
(The Nature Conservancy). We appreciate the funding support from the Endangered
and Threatened Native Flora Conservation Grants Program administered by the Division of
Plant Industry, the National Science Foundation (DEB98-15370, DEB02-33899, DEB08-
12717, DEB-1347843), and the US Fish and Wildlife Service. We thank the Endangered
Plant Advisory Council and Dave Bender (USFWS) for advice and support. This manuscript
was improved by the comments of Christine Bertz and Stephanie Koontz.
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