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INVASION OF CHINESE TALLOW (Sapium sebiferum): A TEST OF DISPERSAL
AND RECRUITMENT LIMITATION IN MULTIPLE HABITATS
A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
UNIVERSITY OF FLORIDA
I thank Doug Levey, Doria Gordon, and Katie Sieving for assistance at all stages of
this proj ect. I am very grateful to lan Renne and Robert Pattison for sharing their
knowledge of Chinese tallow. Stefanie Krantz provided assistance with foraging
observations, and moral support during all stages. I also am grateful to Jim Weimer and
the staff at Paynes Prairie Preserve State Park for making this study possible. Funding
was generously provided by the Florida Department of Environmental Protection, the
Florida Exotic Pest Plant Council, and a University of Florida Alumni Fellowship.
Finally, I would like to thank my parents, who have always encouraged my interests in
TABLE OF CONTENTS
ACKNOWLEDGMENT S ............ ...... ._._ .............._ iii..
LI ST OF T ABLE S ........._.._ ..... .___ .............._ vi...
LIST OF FIGURES .............. ....................vii
AB S TRAC T ......_ ................. ..........._..._ viii..
1 GERMINATION OF CHINESE TALLOW (Sapium sebiferum): THE EFFECTS
OF HABITAT AND DISPERSAL METHOD ON ESTABLISHMENT ............_.....1
Introducti on ............ ......_ ...............1....
M ethods .............. ...............3.....
Study Species............... ...............3.
Study Site................ .. ..... ............
Seed Collection and Treatment .............. ...............6.....
Field Germination Experiment .....__.....___ ..........._ .............
Shade-house Germination Experiment .....__.....___ ........... ..............
Seedling Establishment .............. ...............9.....
Effects of Forest Litter. ............ ..... .__ ...............10..
Statistical Analyses ............ ......_ ...............11....
R e sults.............. ......._ ...............12...
Field Germination................ .............1
Shade-house Germination .............. ...............12....
Seedling Establishment .............. ...............13....
Effects of Forest Litter. ............_...... ...............14..
Discussion .............. ...._ ...............14....
Germination Experiments............... ..............1
Seedling Establishment .............. ...............17....
Effects of Forest Litter. ............_...... ...............18..
2 IDENTIFYING BARRIERS TO RECRUITMENT FOR CHINESE TALLOW
(Sapium sebiferum) IN TWO FOREST HABITATS ................. .......................25
Introducti on ................. ...............25._ ___.......
M ethods .............. ...............28....
Study Species and Site............... ...............28..
Avian Seed Dispersal .............. ...............29....
Point Counts .............. ...............30...
S eed-pred ation Experiment ................. .......... ......... .............
Seed Germination and Establishment............... .............3
Linking the Stages .............. ...............3 3....
Statistical Analyses............... ...............34
Re sults................... .......... ...............36.......
Avian Seed Dispersal .............. ...............36....
Point Counts .............. ...............37...
S eed-pred ation Experiment ................. ...............37.................
Seed Germination and Establishment............... .............3
Linking the Stages .............. ...............3 9....
D discussion ............... .. .. .. .. ...... .......... .............3
Avian Frugivory and Seed Dispersal ....._._._ ......._.. ... .._._ ..........4
Postdispersal Processes .............. ............ ..............4
Recruitment Limitation in Forest Habitats ................ ................ ......... .44
LIST OF REFERENCES ........._... ........... ...............54....
BIOGRAPHICAL SKETCH .............. ...............63....
LIST OF TABLES
2-1 Bird species seen visiting six Sapium sebiferum trees during 106.5 hours of
observation between 6 October 2002 and 25 February 2003, Paynes Prairie
Preserve State Park, Alachua County, FL ................ ...............49...............
2-2 Frugivorous bird species detected on point counts in oak hammock and mixed
pine-hardwood habitats between 12 October 2002 and 5 March 2003, Paynes
Prairie Preserve State Park, Alachua County, FL .............. ....................5
LIST OF FIGURES
1-1. Map of the research field site at Paynes Prairie Preserve State Park, Alachua
County, Florida ................. ...............21.................
1-2. Mean proportion (+ 1 SE) of seeds that germinated............... ...............2
1-3. Germination rate in the shade-house represented as the cumulative proportion of
seeds germinating over time ........._._._ ...._._ ...............23...
1-4. Mean proportion (+ 1 SE) of germinated seeds that established in the field
(FOWP and FSWP) and shade-house (SOWP and SSWP) .............. ...................24
2-1. Sapium seed survivorship in shaded wet prairie (SWP), open wet prairie (OWP),
oak hammock (OH), and mixed pine-hardwood (MPH) habitats at Paynes Prairie
Preserve State Park, Alachua County, FL ................ ...............51...............
2-2. Mean proportion of Sapium seeds (A SD) that germinated ........._.._.. .. ......_.._......52
2-3. Spatial dynamics of recruitment through seedling establishment for Sapium
sebiferum in shaded wet prairie (SWP), open wet prairie (OWP), mixed pine-
hardwood (MPH) and oak hammock (OH) ................. ............... ....___.....53
Abstract of Thesis Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Master of Science
INVASION OF CHINESE TALLOW (Sapium sebiferum): A TEST OF DISPERSAL
AND RECRUITMENT LIMITATION IN MULTIPLE HABITATS
Chair: Douglas Levey
Major Department: Zoology
Biotic invasions are a leading threat to native flora and fauna throughout the world.
Invasive exotic plants are especially widespread, and many benefit from mutualistic
relationships with native fauna that help disseminate their pollen and seeds. Chinese
tallow (Sapium sebiferum) is an exotic species in the southeastern USA that is readily
dispersed by birds, and invades a wide diversity of habitats. However, it is absent in
north Florida from several forest habitats that have been invaded elsewhere in its
non-native range. I investigated seed dispersal, postdispersal seed predation,
germination, and seedling establishment to identify barriers to recruitment in mixed pine-
hardwood and oak hammock forest at a north Florida site where S. sebiferum is absent.
The same data were collected in adj acent shaded and open wet prairie habitats, where S.
sebiferum is invading. Twenty-one bird species dispersed seeds away from parent trees,
and birds often flew into forest habitats after foraging in S. sebiferum trees. These
species were frequently detected on point counts within the forest habitats. Together,
these results suggest that dispersal limitation is not responsible for the failure of this
species to invade the forest habitats at my site. Likewise, postdispersal seed predation
cannot explain the failure of S. sebiferum to invade the forest habitats, because predation
was significantly higher in the prairie habitats. Germination, however, was nearly absent
in the forest, but readily occurred in the prairie; replication of the germination experiment
in a shade-house produced the same results. Thus, germination is a barrier to
establishment in mixed pine-hardwood and oak hammock forests, likely due to a thick
litter layer on the forest floor.
GERMINATION OF CHINESE TALLOW (Sapium sebiferum): THE EFFECTS OF
HABITAT AND DISPERSAL METHOD ON ESTABLISHMENT
Biotic invasions have received considerable attention from ecologists working in
both applied and theoretical contexts. From an applied perspective, invasive exotic
species are second only to habitat loss and degradation as a threat to native species
(Wilcove et al. 1998), and are estimated to cause as much as $138 billion in annual
damages within the United States alone (Pimentel et al. 2000). From a theoretical
perspective, the impact of invasions tests our understanding of community assembly
rules, rates of dispersal, and competition (Parker et al. 1999, Mack et al. 2000).
Plants represent one of the most abundant and well-studied groups of invasive
exotics, partly due to the intentional introduction of many plant species for use as food
and ornamentals (Reichard and White 2001, Mack and Erneberg 2002). Numerous
studies have sought to identify the most important factors that promote or prevent plant
invasions. These include native-species diversity (Elton 1958, Levine and D'Antonio
1999, Naeem et al. 2000, Kennedy et al. 2002), disturbance (Burke and Grime 1996,
D'Antonio et al. 1999, Jesson et al. 2000), and a lack of natural herbivory (Keane and
Crawley 2002). In addition, many studies have attempted to identify a unified suite of
attributes that invaders possess. This approach has resulted in limited predictive power
(Mack et al. 2000), because successful invasion may often depend more on the condition
of the community being invaded than on particular traits of the invader (Myers 1983,
Ewel 1986). Even so, general knowledge of a species' invasive potential and community
invasibility may still not give us the power to predict which plant species are most likely
to invade particular communities (Crawley 1987, Williamson 1996, Lonsdale 1999).
When populations of invasive plants lie adj acent to communities that have not been
invaded, either propagules are failing to arrive, or those that do arrive are limited by
inappropriate biotic or abiotic environments. These mechanisms (termed dissemination
and establishment limitation respectively) are not mutually exclusive, and both may
simultaneously limit plant recruitment (Schupp et al. 2002). Successful identification of
the stages that limit recruitment must therefore consider both dispersal and postdispersal
processes, since the relative importance of any one stage may be reduced or enhanced by
another (Jordano and Herrera 1995, Nathan and Muller-Landau 2000). This approach
can be used to identify habitats that are at most risk of being invaded, and to identify
stages in an exotic species' life cycle that are most susceptible to management and
I used this approach to ask why an invasive tree, Chinese tallow (Sapium sebiferunt
(L.) Roxb.), Euphorbiaceae (hereafter Sapium) is failing to establish in forest habitats that
have been invaded elsewhere in its non-native range. In coastal South Carolina, Sapium
has successfully invaded mixed pine-hardwood and other upland forest habitats (Renne
2001, Renne et al. 2001). In north central Florida, however, it is conspicuously absent
from these habitats, even though it is widespread in many other habitats that are often
adj acent to forests. An investigation of each stage in the recruitment process revealed
that germination is the principal stage preventing establishment of Sapium in these
habitats at a Florida field site (Samuels, unpublished), and litter and duff on the forest
floor may be responsible. Thus, it was important to ask what factors influence this
process, and how they vary among habitats. Here I focus on germination and the related
process of seedling establishment in both prairie (invaded) and forest (noninvaded)
habitats to address the following questions: (1) how does seed treatment (acid-treated to
simulate gut passage, and water-soaked to simulate water dispersal) affect germination
patterns in prairie sites; (2) how does the presence of litter affect germination in forest
and prairie habitats; (3) how does herbivory influence seedling establishment and
survivorship in the prairie habitats; and (4) does litter vary from a South Carolina forest
site where Sapium readily invades, to a Florida forest site where it is absent?
Chinese tallow tree (Sapium sebiferunt) is native to eastern Asia, where it has been
cultivated for approximately 14 centuries to supply soaps, waxes, fuels, dyes, and protein
meal (Scheld et al. 1984, Jones and McLeod 1989, Jubinsky and Anderson 1996, Bruce et
al. 1997). It has been established in the United States for over 200 years, and has become
an invasive species of concern through much of the southeast (Jubinsky and Anderson
1996, Bruce et al. 1997). It is especially invasive in the coastal prairies of Texas, where
it has formed monospecific woodlands in areas that were formerly treeless (Bruce 1993,
Bruce et al. 1995, Barrilleaux and Grace 2000).
In Florida, Sapium flowers from March to May. Flowers occur on a spike-like
thyrse, and are insect pollinated (Nijjer et al. 2002). The fruits are three-lobed capsules
that dehisce from September to November. The white aril that covers the seeds is the
source of the name "tallow," providing a rich source of food for birds. While many
species of birds have been observed feeding at Sapium trees, their quality as seed
dispersers varies depending on seed-handling behavior (Renne et al. 2000, Conway et al.
2002a, Renne et al. 2002). There is also evidence that seeds are dispersed by water
(Bruce et al. 1997), since the waxy aril aids in flotation. Large Sapium trees may produce
nearly 100,000 seeds in a season (Renne et al. 2000), with a mean mass of 0. 121 g
+ 0.002 SE (N = 100; without aril). Germination occurs in a wide variety of habitats
(Renne et al. 2001), although Sapium seeds may require some soaking to achieve
maximum germination success (Conway et al. 2000). Exposure to cold temperatures or
fluctuating temperatures may increase germination success (Cameron et al. 2000, Nijj er
et al. 2002). Sapium seedlings are tolerant of a wide range of environmental conditions,
including moderate flooding (Jones and Sharitz 1990) and heavy shade (Jones and
McLeod 1989). Seedlings appear to be moderately tolerant of soil salinity, which helps
explain the species' success in environments prone to coastal flooding (Conner 1994).
However, elevated soil salinity may result in deleterious effects (Barrilleaux and Grace
2000). Finally, despite the dominance of Sapium in many of the habitats where it has
invaded, there is little evidence this success is due to allelopathic effects (Keay et al.
2000, Conway et al. 2002b).
I worked at two sites separated by 2 km, both within Paynes Prairie Preserve State
Park (Figure 1-1), an 8500 ha natural area in Alachua County, Florida (290 36' N, 82o 20'
W, 25 m). The mean air temperature ranges from 13oC in January to 27oC in August.
Mean annual precipitation is 1370 mm, with the wettest months in June through
September. The preserve contains many biological communities, with basin marsh
representing the largest and most extensive (FDEP 2001). Sapium has successfully
invaded some areas of basin marsh, but suffers high mortality in areas where flooding
persists for long periods of time (J. Weimer, pers. comm.). It is most abundant in the wet
prairie community that lies between the basin marsh and adj acent forests that rim the
This study was conducted in four habitats within the preserve: two where Sapium is
currently invading (shaded wet prairie and open wet prairie); and two adj acent habitats
where it is absent, but has been found elsewhere in its non-native range (mixed pine-
hardwood and oak hammock). The two invaded prairie habitats are similar in vegetative
composition, but differ in structural complexity. Open wet prairie is dominated by a
thick understory of sand blackberry (Rubus cuneifolius) and saltbush (Baccharis
halimifolia), with a canopy that rarely exceeds 2 m. Scattered clumps of persimmon
(Diospyros virginiana) and Sapium represent the only large trees. The shaded wet prairie
also has a thick understory composed mostly of saltbush (Baccharis halimifolia), dog
fennel (Eupatorium capillifolium), elderberry (Samnbucus canadensis), and winged sumac
(Rhus copallina); but has a tree canopy that ranges from 5-10 m. Dominant trees include
persimmon (Diospyros virginiana), sweetgum (Liquidambar~~~dddd~~~~ddd styraciflus), and Sapium.
These two habitats freely grade into each other via a "soft edge," and are best separated
by canopy height. Dominant soils of the prairie habitats include Wauberg Sand (a poorly
drained loamy siliceous soil) and Shenks Muck (a poorly drained clayey montmorillonitic
soil; Thomas et al. 1985).
Study sites where Sapium is absent were mixed pine-hardwood and oak hammock.
These habitats freely grade into each other, yet form an abrupt "hard edge" with the
adjacent prairie habitats. Mixed pine-hardwood is dominated by loblolly pine (Pinus
taeda), live oak (Quercus virginiana), and sweetgum (Liquidambar~~~dddd~~~~ddd styraciflus), with
scattered water oaks (Quercus nigra) in the understory. The oak hammock is more
diverse than the mixed pine-hardwood, but is dominated only by live oak (Quercus
virginiana). Other common tree species include laurel oak (Quercus laurifolia), water
oak (Quercus nigra), sugarberry (Celtis laevigata), southern magnolia (Magnolia
grandiflora), and American holly (Ilex opaca). Yaupon holly (Ilex vomitoria) and Vitis
sp. are common in the understory. Dominant soils of the two forest habitats include
Myakka Sand and Newnan Sand, both somewhat poorly drained sandy siliceous soils
(Thomas et al. 1985).
In 2003, the density of Sapium > 3 cm dbh was 465 plants/ha in the prairie habitats,
verses 0 plants/ha in the forest habitats (15 points/habitat; point-quarter method, Brower
et al. 1990). Sapium is present in the prairie habitats up to the edge of the forest habitats,
including the narrow ecotone that divides prairie from forest.
Seed Collection and Treatment
In December 2002, I collected approximately 2500 Sapium seeds from 12 different
trees, eight of which grew in open wet prairie and four in shaded wet prairie. I attempted
to collect seeds from a diversity of positions on each tree, since maternal investment may
vary with position, which can affect germination patterns (Baskin and Baskin 1998).
Seeds were brought to the laboratory and treated the same day of collection in two ways,
hereafter referred to as acid-treated and water-soaked seeds. These treatments reflect the
two ways that Sapium seeds may be dispersed. Acid-treated seeds mimic those that are
ingested by birds and may arrive in all four habitats via avian dispersal. In contrast,
water-soaked seeds mimic those dropped by birds or that fall from trees in the prairie
habitats, where flooding periodically occurs and water dispersal is possible. Therefore,
use of water-soaked seeds is restricted to germination experiments in the prairie sites.
Approximately 1600 (66%) of the collected seeds were acid-treated. These seeds
were initially soaked in water for five hours to loosen the waxy aril that covers the seed,
followed by 20 minutes of soaking in pH 2.0 HCL. This approximates the hydrogen ion
concentration in the gizzard of a bird, where the lowest pH is expected (Sturkie 1976).
The aril was then removed by agitating seeds between two layers of aluminum screening,
applying enough pressure to ensure removal of the aril, but not enough to damage the
seed coat. Acid-treated seeds were returned to the field and stored under cages (to
prevent predation) in each of the four respective habitats until the germination experiment
was initiated. This ensured that seeds were subj ected to conditions of natural
cold-stratification. No seeds germinated during storage.
The remaining 33% of the seeds were water-soaked with the aril intact in an
eight-gallon bucket for one month between December and January. The bucket was kept
outside in the shade during the entire soaking period to ensure that seeds would be
subj ected to natural temperature fluctuations, and water was changed once after two
weeks of soaking. Most of the seeds floated when initially placed in the water, but
gradually began to sink when the aril became saturated.
Field Germination Experiment
I conducted field germination experiments to evaluate the combined effects of
habitat and seed treatment on germination. In January 2003, I selected 48 sites, 12 in
each of the four habitats (open wet prairie, shaded wet prairie, oak hammock, and mixed
pine-hardwood). Sites were located at 30 m intervals along two transects in oak
hammock and open wet prairie, and three transects in mixed pine-hardwood and shaded
wet prairie. I used existing trails to access sites, but placed seeds at least 30 m from the
nearest trail. Vegetation structure prevented me from placing transects in random
Acid-treated seeds were removed from field storage cages and at each site, 16 seeds
were placed on the ground in four groups of four, each group placed one meter from a
center point in each of the four cardinal directions (n = 192 seeds/habitat). Four is a
typical number of seeds in a bird defecation (I. Renne, pers. comm.). Seeds were placed
on the surface of the soil (or leaf litter when present) to mimic the state of a recently
dispersed seed. To prevent the loss of seeds from mammalian seed predators, I initially
covered each group of four seeds with a cage (8x8x6 cm) made from 0.25 inch (23
gauge) galvanized wire mesh.
After one month, water-soaked seeds were removed from the bucket and
immediately placed in the field to evaluate germination. Water-soaked seeds were placed
at the same sites as the acid-treated seeds in the shaded and open wet prairie habitats.
Acid-treated and water-soaked seeds were placed side by side under separate cages.
Seeds were checked once per week starting in January 2003, and ending when
germination had ceased (i.e., when the cumulative percent germination curve had reached
a plateau). Germination was defined as a split seed coat and/or emergence of the radicle.
Shade-house Germination Experiment
Both the acid-treated and water-soaked experiments were replicated in a
shade-house to provide greater consistency with respect to watering regime and light
environment. The shade-house had a 240 X 120 cm base with 60 cm between the
germination platform and the top. The top was covered with 62-70% shade-cloth to
prevent direct exposure to the sun and to better simulate the shaded environment where
most seedlings naturally occur. In addition, clear plastic was placed over the shade-cloth
to prevent natural precipitation from reaching the seeds. The shade house was located on
the roof of Carr Hall, University of Florida (290 3 8.626' N, 82o 20.694' W).
In December 2002, soil was collected from the upper 10 cm of the soil surface in
each of the four habitats. In addition, litter and duff were collected from the two forest
habitats. In the laboratory, soil from each habitat was thoroughly mixed, and randomly
allocated to 100 mL cell packs with perforated bases. For the two forest habitat
treatments, small amounts of litter and duff were applied to the surface of the soil in an
attempt to simulate the presence of this vegetative material on the forest floor. Most
experimental sites in the prairie were characterized by exposed soil and only a thin layer
of leaf litter. Thus, no attempt was made to recreate the presence of litter on prairie soils
in the shade-house. I placed four seeds/cell on the surface of the soil (n = 144
seeds/habitat-soil type), and cut holes in the potting trays onto which cell packs were
placed to allow drainage. Cells were watered to saturation every 5 days from December
through March, and every 4 days from April until May 20, 2003 when additional
germination was no longer detected and the experiment was terminated. Potting trays
were randomly shifted each time they were watered to control for placement effects.
Seeds were checked for signs of germination every four days, and germinated seeds were
marked with color-coded toothpicks to identify the date of germination.
The fate of germinated seeds was followed to evaluate the effect of habitat on
seedling establishment. In the field germination experiment, wire cages were removed
only when a Sapium seedling was about to touch the top of the cage (6 cm tall). The
position of the established seedling was then marked, and the remaining seeds were
moved and re-caged approximately 0.25 m from the original site so their fate could be
monitored for the remainder of the germination experiment. This process was repeated
for all seeds that germinated and established. After the germination experiment was
terminated in May 2003, the heights of surviving seedlings were measured every 10 days,
and the relative degree of herbivory (minor, moderate, heavy) was noted to explore
habitat specific differences in the cause and extent of seedling mortality. All remaining
seedlings were pulled from the ground and destroyed at the end of August 2003.
In the shade-house, established seedlings were pulled when they reached 10 cm
height. Seedlings were dried overnight at 60oC and above ground dry mass weighed to
0.001 g. I did not measure below-ground biomass because the roots of some seedlings
broke during extraction. This experiment was terminated on May 20, 2003, at which
time seedlings were showing signs of physical stress. Seedlings that had not reached
10 cm by this date were not used in subsequent analyses.
Effects of Forest Litter
Because litter and duff on the forest floor appeared to affect germination success, I
compared this attribute at Paynes Prairie to the Hobcaw Forest in South Carolina where
Sapium has invaded forest habitats. The 3077 ha Hobcaw Forest (33o 20'N, 790 15' W) is
located on the outer coastal plain in Georgetown County, South Carolina. Mean annual
precipitation is 1315 mm, and mean air temperature ranges from 90C in January to 27oC
in August. The Hobcaw Forest contains a variety of habitats that are similar to those
found at Paynes Prairie, although it lacks the large basin marsh. In contrast to Paynes
Prairie, however, Sapium has successfully invaded mixed pine-hardwood, loblolly pine
forest, and other oak dominated forests at the Hobcaw site.
In August 2003, I randomly placed ten 30 m transects in mixed pine-hardwood
forest at the Hobcaw field site. This procedure was repeated in September 2003 in mixed
pine-hardwood at Paynes Prairie. I did not assess litter in oak hammocks, since a
comparable forest type was not adequately represented at the Hobcaw site. Litter depth
was measured at 3 m intervals along each transect by inserting a thin wooden rod through
the litter until it stopped at the soil surface. At the mid-point of each transect, I placed a
0.25 m2 quadrat on the ground, and collected all of the litter within the square. Litter was
dried at 60oC and weighed to 0.01 g.
Because very few seeds germinated in the oak hammock and mixed pine-hardwood
habitats, germination results did not meet parametric assumptions of normality and equal
variance. Therefore, germination success for both the field and shade house experiments
was compared among treatments with a Kruskal-Wallis test, where the response variable
was the proportion of seeds that germinated per site (Hield) or per cell (shade-house). I
used the Nemenyi test, a Tukey-type multiple comparison procedure, to detect significant
differences among treatments (Zar 1999). Germination rate, the cumulative number of
seeds that germinated over time, was compared among treatments for the shade-house
experiment with a 2-sample Kolmogorov-Smirnov test. Germination rate was not
determined in the field since some seeds could not be located until the experiment was
terminated, and for them, it was impossible to determine when the seed coat had split.
The mass of dried seedlings from the shade-house was compared using 1-way ANOVA.
For the comparison of litter depth and mass between Paynes Prairie and the Hobcaw
Forest, I used a one-sided t-test. This was based on the a priori expectation that litter
depth at Paynes Prairie was greater, because germination occurred on Paynes Prairie
forest soils in the absence of litter (Samuels, unpublished). Thus, I was testing the
prediction that less litter was present at the Hobcaw Forest site. All analyses were
calculated using SPSS 10.0 (SPSS Inc., Chicago, IL) and Minitab 12.0 (Minitab Inc.,
State College, PA), and means are reported & SE, with a = 0.05.
Seeds placed in the field in December began to germinate at the end of February
2003, and germination peaked in March. Germination success in the Hield varied widely
among the four habitats and between the two seed treatments (Figure 1-2A). Within each
prairie habitat, germination success of water soaked seeds was significantly higher than
acid treated seeds (H = 53.79, df = 5, P < 0.001), but water soaked treatments did not
differ significantly between the two prairie habitats. Only one seed germinated in mixed
pine-hardwood (MPH), while no seeds germinated in oak hammock (OH). Mean
germination success for acid treated seeds was higher in shaded wet prairie (SWP) than
open wet prairie (OWP), x = 0. 19 & 0.04 verses 0. 10 + 0.05 respectively, but OWP did
not differ significantly from OH, MPH, or SWP (Figure 1-2A).
As with the Hield experiment, seeds began to germinate in the shade-house in late
February 2003, peaking in March. The pattern of germination success was very similar
to that observed in the Hield (Figure 1-2B). The mean proportion of acid treated seeds
that germinated on OWP soil was comparable to that for SWP (x = 0. 14 & 0.03 and
0.18 & 0.04, respectively). Acid-treated seeds in OH and MPH showed significantly
lower germination than did acid-treated seeds in OWP and SWP, which in turn had lower
germination than the water soaked seeds placed on the two prairie soils (H = 94. 15,
df = 5, P < 0.001). Two seeds germinated in OH, and only one in MPH.
On the prairie substrates, germination rate was primarily affected by seed
treatment, but water-soaked seeds were also affected by soil substrate. Water-soaked
seeds showed a burst of germination in late February, approximately 65 days after sowing
(Figure 1-3). However, the rate of germination for water-soaked seeds in SWP was still
significantly higher than that for water-soaked seeds in OWP (Z = 1.945, n = 118,
P = 0.001). The difference in germination rate between acid-treated seeds for the two
prairie soils was not significantly different (Z = 1.237, n = 46, P = 0.094).
Of those seeds that successfully germinated (n = 213 in Hield, 168 in shade-house),
a significantly larger proportion established in the shade-house than in the field
(H = 1 1.26, df = 3, P = 0.01; Figure 1-4). A total of 25 seedlings (1 1.7%) initially
established in the Hield (7 in OWP and 18 in SWP) compared to 69 seedlings (41.1%) in
the shade-house (29 in OWP, 38 in SWP, 1 in OH, and 1 in MPH). Of the 213 seeds that
germinated in the Hield, 53% were predated by fire ants (Solenopsis invicta), while most
of the remaining seeds that germinated but did not establish appeared to die from
desiccation. Of those that established as seedlings in the field, 15 were still alive by the
end of May 2003. Mean seedling height was 12.2 + 1.3 cm, and most showed some signs
of herbivory. By the end of August only five were still alive. The fate of most of the
seedlings was either attributed to herbivory (60%), or unknown causes (40%). Seedling
death was attributed to herbivory when heavy leaf damage was noted on one visit, and the
bare, leaf-less stem of the seedling was found on a subsequent visit. In the shade-house,
seedlings reached 10 cm (and were pulled) in as little as 20 days. Only four seedlings
died between the date of first establishment and termination of the experiment. The
cause of death was unknown, although herbivory was absent within the shade-house.
Mean above ground dried mass of 10 cm seedlings ( x = 0.086 & 0.004 g) did not differ
among the two prairie soils for either acid-treated or water-soaked seeds (F3,40 = 1.25,
P = 0.304).
Effects of Forest Litter
Litter at both sites (Hobcaw Forest and Paynes Prairie) was dominated by pine
needles. As expected, there was a significant correlation between litter depth and mass
(Flrls = 23.99, r2 = 0.57, P < 0.001; linear regression). Mean litter depth at the Hobcaw
Forest was significantly less than Paynes Prairie (2. 17 & 0.30 cm verses 3.17 & 0.40 cm;
t = -2. 10, df = 18, P = 0.03).
The high germination success of water-soaked seeds cannot explain the significant
difference among acid-treated seeds sown in the prairie verses forest habitats. In both the
field and the shade-house, there was virtually no germination for the oak hammock or
mixed-pine hardwood sites, suggesting that germination is the leading barrier to
establishment in these habitats where Sapium is currently absent. Lack of germination
alone cannot explain the failure of Sapium to invade the forest habitats because of the
independence among stages in the recruitment process, and the outcome of one process
obscuring or enhancing the effects of another (Jordano and Herrera 1995). However, in a
parallel study at the same time and site (Samuels, unpublished) I quantified both dispersal
and seed-predation and the results indicate that germination is the process most
responsible for preventing initial establishment in oak hammock and mixed
The great similarity between field and shade-house results demonstrates both the
success of the shade-house in mimicking field conditions, and the important effects of
litter and seed treatment on germination when watering regime and light conditions were
held constant. Seeds were placed on the surface in all treatments to mimic the state of
seeds that had recently been dispersed by a bird or (in the case of water-soaked seeds)
had recently arrived via water dispersal. The 15% germination success of acid-treated
seeds in the two prairie habitats (field and shade-house) was comparable to the 20%
observed by Renne et al. (2001) for bird-defecated seeds placed on the surface of
vermiculite in a greenhouse environment. Several studies have evaluated germination
only for buried Sapium seeds, and often without any attempt to mimic avian gut passage.
Burial of untreated Sapium seeds resulted in germination success of 52.4 + 5.9%
(Cameron et al. 2000), but seeds in this study were stored for six years prior to sowing.
Less than 20% germination success was observed by Bruce (1993) in grassland and
Sapium woodland for seeds that were untreated and placed on the soil surface. However,
the combined effect of avian gut passage and seed burial may increase germination
success to as much as 80% (Renne et al. 2001), with acid-treated seeds showing similar
emergence patterns to defecated seeds.
While germination success might have been improved through seed burial, burial is
not likely immediately following bird dispersal. In the prairie habitats, however, water
may provide an alternative means of dispersal after heavy rains, and germination success
of water-soaked seeds greatly exceeded that of acid-treated seeds both in the field and the
shade-house. Conway et al. (2000) soaked Sapium seeds in water (for 6, 20, 48, and 72
hours) and found germination success to be much lower than water-soaked seeds in my
study. Most of their results (which combined the effect of soaking duration with chilling)
showed a mean germination success of only 3.33%. The great difference with the present
study is likely due to soaking duration (30 days verses 3 days maximum), and the
germination environment used by Conway et al. (2000), which involved petri dishes as
the germination substrate that were then placed in a germination chamber.
Water dispersal for Sapium is mentioned in the literature (Bruce et al. 1997), but
has not been rigorously examined. Hydrochory may be the optimal mode of dispersal in
seasonally flooded habitats, while ornithochory still ensures that Sapium seeds can arrive
in habitats where water dispersal is not possible. The maintenance of such different
dispersal mechanisms likely diversifies the range of dispersal distances (Williamson and
Costa 2000). Thus, water appears to play a key role in the maintenance and spread of
Sapium in the prairie habitats, while the absence of flooding in the forest reduces the
chance of Sapium establishment. For seeds that do arrive in the forest, however,
germination appears to be the leading barrier to recruitment.
The much higher germination success in prairie than forest habitats may be due to a
thick layer of litter, which is dominated by leaves in oak hammock, and by pine needles
in mixed pine-hardwood. Most of the seeds, which were placed on the surface of the
litter, remained within or on top of a layer of vegetation that quickly dried after rainfall.
Thus, seeds were rarely in a moist microenvironment long enough to promote imbibition.
This conclusion is further supported by the observation that the only seed that germinated
in the forest (mixed pine-hardwood) was located in a spot where water pooled after a
heavy rain, and the seed became trapped among wet leaves. Furthermore, the only
shade-house seeds that germinated for the two forest habitat treatments had dropped
below the layer of litter and duff applied to their cells, and were thus in contact with
moist soil. Burial of seeds in moist forest soil probably would have increased
germination success. An alternative explanation is that the forest habitats buffer against
temperature fluctuations, since germination success of Sapium may increase with
fluctuating temperatures (Nijjer et al. 2002). However, this mechanism seems unlikely
since temperature fluctuations were consistent among treatments in the shade-house.
Furthermore, germination did take place in the shade-house on soil collected from both
oak hammock and mixed pine-hardwood, when no litter/duff was applied (Samuels,
The relationship between seed germination and seedling establishment was far
from 1:1, especially in the field. Given that only 1 1.7% of germinated seeds successfully
established in the field, equating germination with establishment would be misleading.
The lower field establishment than in the shade house (41.1%) is best explained by (1)
the foraging activity of fire ants (Solenopsis invicta), and (2) periodic dry conditions,
both of which were absent in the shade-house.
Bisected seed coats initially revealed foraging activity by S. invicta. In contrast,
mammalian predators leave splintered and haphazardly broken seed coats (Samuels,
unpublished). Furthermore, seeds in the field germination experiment were protected
from mammalian predators by cages. I later encountered S. invicta swarming recently
germinated seeds and consuming the endosperm entirely. This observation is consistent
with the foraging activity of S. invicta in many agricultural systems of the southeast USA
(Morrison et al. 1997), where ant activity can also result in reduced seedling vigor,
damage to cotyledons, and an increase in malformed seedlings (Shatters and
Vander Meer 2000). Ready and Vinson (1995) found that small seeds are moved and
damaged more often than large seeds by S. invicta, and that the seed coat may protect
some seeds from attack. This is also consistent with my observation that ants were never
seen associating with intact (ungerminated) seeds, which are too large for S. invicta to
carry and too hard to penetrate.
During the field germination experiment (Jan-May), there was considerable
variation in monthly precipitation; mean = 88.0 mm + 39.4. This resulted in days when
some cages that protected seeds were subj ected to moderate flooding, followed by shorter
periods without rain when the ground was dry. Seeds placed on the soil surface are likely
to be much more sensitive to such climatic fluctuations than buried seeds. Desiccation of
germinated seeds appeared to be a common cause of mortality, second to ant predation.
Overall, the placement of seeds on the surface is likely the main reason that establishment
in the field was lower than that observed by Renne et al. (2001). In the shade-house
(where I watered seeds every 4-5 days and ants were absent) it is less certain why
establishment of germinated seeds was still < 50%.
Effects of Forest Litter
In seed introduction studies, recruitment following seed addition indicates the
presence of a regeneration niche for that species, and may be a sign of dispersal limitation
(i.e., seeds are failing to arrive at suitable microsites; Turnbull et al. 2000). The near
absence of germination in the forest sites at Paynes Prairie combined with the observation
that avian dispersers carried seeds to these sites (Samuels, unpublished) implicate
postdispersal processes as the most likely barrier to establishment. At the Hobcaw Forest
in South Carolina, mean litter depth was significantly less than at Paynes Prairie, and
Sapium readily established under a mixed pine-hardwood canopy. Seedlings of Sapium
that had recently emerged from the litter were seen adj acent to transects at the Hobcaw
site, as were larger saplings and adult plants. In contrast, no Sapium plants of any ages
were encountered along transects in mixed pine-hardwood at Paynes Prairie.
The effects of litter on germination and establishment have received considerable
attention, and the response is often mixed and species specific (Molofsky and Augspurger
1992, Facelli 1994, Hastwell and Facelli 2000, McAlpine and Drake 2003). Inhibition of
germination and/or establishment by litter may be indirect through alteration of habitat
for seed predators, or changes in exposure to solar radiation. Allelopathic effects due to
litter leachates are also possible (Barritt and Facelli 2001). Deep litter may also result in
seedling desiccation if seeds germinate without contact with soil (Fowler 1988). It is
unknown which, if any, of these factors may play in role in preventing Sapium from
establishing in oak hammock and mixed pine-hardwood at Paynes Prairie; establishment
in these forest habitats was never evaluated because germination was negligible. In
general, however, litter has a stronger overall effect on seed germination than seedling
establishment, and litter-reducing disturbances may facilitate germination in some
systems (Xiong and Nilsson 1999). One such disturbance that differs between Paynes
Prairie and the Hobcaw Forest is fire.
Fire has been suppressed at the forest sites at Paynes Prairie for many years, in part
due to a residential area that borders the park. In contrast, prescribed fire is regularly
used at the Hobcaw Forest. This recurring disturbance reduces litter and duff every three
to five years, which may open windows of opportunity for Sapium seeds to germinate.
Fire may have direct effects through stimulation of germination via heating of the soil
surface where seeds are present (Tyler 1995). Alternatively, indirect effects of fire may
induce germination by removing litter, and manual removal of litter has successfully
imitated this disturbance in some studies (Lambert and Menges 1996, McConnell and
Menges 2002). If fire were restored to the forest habitats of Paynes Prairie State Park,
Sapium might be able to expand its distribution there.
In summary, my results show that seeds of S. sebiferunt fail to germinate in oak
hammock and mixed pine-hardwood at a north Florida field site. At the same time,
Sapium may benefit from both bird-dispersal and water-dispersal in wet prairie habitats,
where flooding occurs. The geographic extent of Sapium invasion in the southeast USA
remains to be seen. In north Florida, however, postdispersal processes rather than
dispersal limitation currently prevent Sapium from establishing in some forest habitats.
Large-scale disturbances that can reduce litter may create windows of opportunity for
Sapium to invade if other microsite conditions are suitable for establishment.
0 0.20.4 0.8 1.2 1.6
Figure 1-1. Map of the research field site at Paynes Prairie Preserve State Park, Alachua
AMPH AOWP ASWP WOWP WSWP
AOH AMPH AOWP ASWP
Figure 1-2. Mean proportion (+ 1 SE) of seeds that germinated. A) In the field. B) In
the shade-house. Acid-treated seeds were placed in oak hammock (AOH),
mixed pine-hardwood (AMPH), open wet prairie (AOWP) and shaded wet
prairie (ASWP). Seeds soaked in water for one month were only placed in
open wet prairie (WOWP) and shaded wet prairie (WSWP). Treatments with
the same letters above error bars are not significantly different at a = 0.05.
60 80 100 120 140 160
Days after sowing
Figure 1-3. Germination rate in the shade-house represented as the cumulative
proportion of seeds germinating over time. Both acid-treated seeds (AOWP
and ASWP) and seeds soaked in water for one month (WOWP and WSWP)
were placed on soil taken from the two respective prairie habitats.
Germination on the forest habitat soils was insufficient to calculate rate. All
germination curves are significantly different from each other except for
AOWP and ASWP (Z = 1.24, N = 46, p = 0.094; two-sample Kolmogorov-
o 0.2 -a
FOWP FSWP SOWP SSWP
Figure 1-4. Mean proportion (+ 1 SE) of germinated seeds that established in the field
(FOWP and FSWP) and shade-house (SOWP and SSWP). Data are pooled
for acid-treated and water-soaked seeds within each habitat X location
combination. Treatments with the same letters above error bars are not
IDENTIFYING BARRIERS TO RECRUITMENT FOR CHINESE TALLOW (Sapium
sebiferum) IN TWO FOREST HABITATS
Understanding the effects of biotic invasions has become a priority for both
scientists and policy makers. Although we still lack a common framework for
quantifying and comparing the impact of different invaders (Parker et al. 1999), invasive
species as a whole are second only to habitat loss and degradation as a threat to native
organisms in the United States (Wilcove et al. 1998). Unfortunately, human practices of
cultivation and husbandry have increased the chances that many nonindigenous
populations will become established (Mack et al. 2000), and exotic species continue to be
introduced throughout the world.
Invasive plants are perhaps the most conspicuous taxon of nonindigenous
organisms. The high diversity of invasive plant species in many regions is partly due to
the intentional introduction of plants for utilitarian and aesthetic purposes (Mack 2001),
and partly due to the relative ease with which non-native plants develop mutualisms in
their new range (Richardson et al. 2000). Exotic plants with fleshy fruits or those that
offer some form of nutritious reward for seed removal may be easily utilized by
frugivorous animals. Birds in particular have been quick to take advantage of exotic
plants that offer such rewards, with numerous examples of plant invasions assisted by
avian frugivory (Buchanan 1989, White and Stiles 1992, Sallabanks 1993, Figueiredo
1997, Lockhart et al. 1999, Renne et al. 2000, Reichard et al. 2001). If germination fails
to occur without gut passage of seeds, successful invasion may be highly dependent upon
avian frugivores (Panetta and McKee 1997).
Assuming that a given exotic plant species can find mutualistic partners for
pollination, seed dispersal, or mycorrhizal relationships, many other factors may still
determine whether that species can invade. These factors include native plant diversity
(Naeem et al. 2000), disturbance (D'Antonio et al. 1999), the number of times a species is
introduced (Williamson and Fitter 1996), and the environmental conditions of the
community being invaded (Ewel 1986). Studies of exotic plant invasions have often
focused on the spread and impact of these species, and some studies have emphasized the
processes that facilitate invasion from the species level to the community level.
However, little attempt has been made to understand why particularly invasive plants do
not establish in seemingly appropriate habitats where dispersal of seeds may be high.
The spread of such species to these sites may be limited by one or more stages in
the recruitment process. Barriers to recruitment may occur if there is a source limitation
(i.e., seed output is low), if there is dispersal limitation (i.e., seeds fail to arrive at
potential recruitment sites), or if there is establishment limitation (i.e., postdispersal
mortality of seeds or seedlings is disproportionately high; Schupp et al. 2002). All of
these barriers may simultaneously limit recruitment and the establishment of new
populations. Although recruitment cannot occur without seed arrival, seed arrival is no
guarantee of recruitment; postdispersal processes must also be considered to understand
the impact of dispersal agents on recruitment (Nathan and Muller-Landau 2000). By
viewing dispersal as just one event in a sequence, the effect of this stage may be
contrasted with subsequent interactions that follow, thus gauging the relative importance
of dispersal in driving recruitment dynamics (Rey and Alcantara 2000). Such an
integrated approach is especially important, given that the vulnerability of any particular
habitat to invasion may vary from stage to stage in the plant' s life cycle (Schupp and
Fuentes 1995). This independence of processes operating at different stages, or
uncoupling of different stages, can offset or obscure the effects of previous stages
(Jordano and Herrera 1995). The most complete picture of the recruitment process is
therefore provided by studies that explicitly link patterns of seed dispersal to
demographic consequences at all sequential stages (Schupp and Fuentes 1995).
I used this approach to study the invasion dynamics of the exotic tree Chinese
tallow (Sapium sebiferunt (L.) Roxb.), Euphorbiaceae (hereafter Sapium). In coastal
South Carolina, this species regularly invades mixed pine-hardwood forests and oak
dominated forests (Renne et al. 2000, Renne et al. 2001), yet it is conspicuously absent
from these habitats in north central Florida despite the floristic similarities between the
regions. I investigated both dispersal and postdispersal processes at a north Florida site
to ask (1) which bird species are most effective with respect to quantity of Sapium seed
dispersed, and are seeds being dispersed into adj acent forest habitats where Sapium is
absent; and (2) how does postdispersal seed-predation, germination, and seedling
establishment vary among two prairie habitats where Sapium is present, and two forest
habitats where it is absent? Finally, I link together both dispersal and postdispersal
processes as the product of process-specific transition probabilities to identify the stages)
acting as a barrier to recruitment in oak hammock and mixed pine-hardwood forests.
Study Species and Site
Chinese tallow (Sapium sebiferum) was intentionally introduced to the United
States for cultivation over 200 years ago because of its many uses. In China (where it has
been cultivated for 14 centuries) the aril is made into waxes, fuels and soaps, while the
leaves are used for dyes (Scheld et al. 1984, Jones and McLeod 1989, Jubinsky and
Anderson 1996, Bruce et al. 1997). Sapium has become a particularly invasive species in
the southeast USA, especially on the gulf coast of Texas where it has invaded coastal
prairie and created monoculture woodland where previously no forest was present (Bruce
1993, Bruce et al. 1995, Barrilleaux and Grace 2000).
Flowering takes place from March to May in Florida, where this study was
conducted. Inflorescences are in the form of spike-like thyrses, which mature into a 2-3
seeded capsule that dehisce from September through December. The white arillate seeds
are dispersed by a variety of bird species, although there is much variation in the quality
of avian dispersal agents due to seed handling behavior (Renne et al. 2000, Conway et al.
2002a, Renne et al. 2002). It has also been suggested that seeds are dispersed by water
(Bruce et al. 1997), since the waxy aril aids in flotation. Germination may occur in a
variety of habitats (Renne et al. 2001), although cold stratification (Cameron et al. 2000),
fluctuating temperatures (Nijj er et al. 2002), and moisture (Conway et al. 2000) are
abiotic factors that increase germination success. Emerging seedlings are also tolerant of
a wide variety of conditions including moderate flooding (Jones and Sharitz 1990), heavy
shade (Jones and McLeod 1989), and moderate soil salinity (Conner 1994). Despite the
invasiveness of this species, there is currently little evidence of allelopathic inhibition of
other plant species (Keay et al. 2000, Conway et al. 2002b).
This study was conducted in Paynes Prairie Preserve State Park, Alachua County,
Florida. See Chapter 1 for a more detailed description of the park and field sites.
Research took place in four habitats: two prairie habitats where Sapium is present (shaded
wet prairie and open wet prairie); and two forest habitats where it is absent (oak
hammock and mixed pine-hardwood), but where it occurs elsewhere in its non-native
range. The two prairie habitats freely grade into each other, and are best separated by
structural diversity; the shaded wet prairie having more trees. Similarly, oak hammock
and mixed pine-hardwood freely grade into one another, the latter being distinct through
the presence of pines. However, the prairie habitats form an abrupt edge with the forest
Avian Seed Dispersal
In order to determine if seeds were being dispersed to the forest habitats, I
evaluated the relative effectiveness of avian frugivores with respect to the quantity of
seeds they disperse, which is a function of the number of visits made by a disperser and
the number of seeds dispersed per visit (Schupp 1993, Jordano and Schupp 2000). Six
Sapium trees that were comparable in size were selected for observation: three in open
wet prairie and three in shaded wet prairie. Two trees in open wet prairie and one in
shaded wet prairie were located close to the forest edge (< 10 m), while two trees in
shaded wet prairie and one in open wet prairie were located far from the edge (> 100 m).
Only data from close trees (#1-3) were used to calculate transition probabilities of
dispersal (see below) as it was often difficult to determine where birds flew after foraging
in trees far from the edge. However, data from close trees was compared with those from
far trees (#4-5) to verify that visitation rates to close trees were representative of the
population as a whole.
An observer with binoculars was stationed ~ 15 m from a tree, starting 15 minutes
after sunrise and continuing for 1-3 hours on a given day. Bird activity declined
considerably by midmorning, so foraging observations did not extend beyond three
hours. Trees were observed for a total of 106.5 h (x = 17.8 + 1.6 SD h/tree) between
6 October 2002 and 25 February 2003. For each bird that visited, the species, duration of
visit, number of seeds carried, number of seeds ingested, number of seeds dropped, and
direction of postforaging movement were recorded. In addition, it was noted if birds
pecked at seeds, or scraped off the aril without removing seeds from the tree. Foraging
observations were terminated when trees had been depleted of seeds.
To determine which bird species that disperse Sapium seeds in the prairie are also
present in the forest, I used fixed-radius point counts to assess the relative abundance of
seed-dispersing bird species in the two habitats where Sapium is absent (i.e., oak
hammock and mixed pine-hardwood). I used standard bird monitoring protocols (Ralph
et al. 1993, Ralph et al. 1995) to establish 24 fixed-radius point count stations
(50 m radius), 12 in oak hammock and 12 in mixed pine-hardwood. Points were located
approximately 250 m apart, and at least 50 m from the edge of any adj acent habitat type.
The number of points in the mixed pine-hardwood habitats was subsequently reduced to
11 after one station was found to be too close to the prairie-forest edge. A count period
of 5 min was used, during which all birds seen and/or heard were recorded. In
subsequent analyses, I did not include flyovers or species that were never seen ingesting
or carrying Sapium seeds at prairie trees.
I revisited each point seven times during the season when Sapium trees contained
seeds (October-February). For each point count station, I then calculated the mean
number of individuals detected per point per visit for each species. Counts started 15
minutes after sunrise and continued for two hours or less. Points were visited in random
order, and counts were not conducted during inclement weather.
To determine if higher seed-predation might account for the failure of Sapium to
establish in forest habitats, I followed the fate of experimentally placed seeds in the field
over 55 days. In each of the four habitats, twelve sites were systematically spaced 30 m
apart along two transects in oak hammock and open wet prairie, and three transects in
mixed pine-hardwood and shaded wet prairie. I used existing trails to access sites, but
placed seeds at least 30 m from the nearest trail. Vegetation structure prevented me from
placing transects in random locations. In October 2002, approximately 1000 seeds were
collected from eight trees at the site. At 1.0 m distances from the center point of a site in
each of the four cardinal directions, four seeds were placed together on the ground (12
sites X 16 seeds/site = 192 seeds/habitat). Placing seeds on the surface simulates the state
of recently dispersed seeds, and four Sapium seeds are a typical number found together in
a bird defecation (I. Renne, pers. comm.). Prior to placement in the field, seeds were
treated with 2.0 pH HCL to simulate avian gut passage; see Chapter 1 for more complete
seed treatment methods. Forceps were used to place seeds on the ground (taking special
care not to touch seeds with the hands) since human scent can bias seed removal data
(Duncan et al. 2002, Wenny 2002). Each group of four seeds was surrounded by three
toothpicks inserted half way into the ground to facilitate relocation. I visited
experimental sites every three days, and recorded the number of seeds remaining. Prior
to the experiment, I used a Trailmaster@ 550 motion/IR triggered camera to identify seed
predators in the study area.
Seed Germination and Establishment
The same experimental design used in the seed predation experiment was used here
to determine if low germination or lack of seedling establishment might explain the
failure of Sapium to establish in forest habitats. See Chapter 1 for a more complete
discussion of the methods and results of this experiment.
Seeds were collected from 12 trees at the Paynes Prairie Hield sites in December,
2002, and treated in two ways prior to placement in the Hield. I acid-treated 768 seeds
(192/habitat), and soaked 384 seeds with the aril intact in water for one month to simulate
the effects of water dispersal (i.e., immersion in water) on germination. Acid-treated
seeds were stored under cages in the Hield to ensure that seeds were subj ected to natural
The sites where seeds were placed in the seed predation experiment were moved
3 m in a random direction to avoid disturbed ground. In late January, acid-treated seeds
were reallocated to each of these new experimental sites in all four habitats, and covered
with a cage (8x8x6 cm) made from 0.25 inch (23 gauge) galvanized wire mesh, to
prevent predation. Seeds were placed on the surface to simulate the condition of a
recently dispersed seed. At this time, water-soaked seeds were sown under separate
cages adj acent to acid-treated seeds in the two prairie habitats (192 seeds/habitat).
Water-soaked seeds were only sown in the prairie habitats, since water dispersal would
not be expected in the forest habitats at this site where flooding does not occur.
Seeds were monitored weekly for signs of germination (split seed coat and/or
emergence of the radicle). The cage was removed only when an established seedling was
near the top of a cage. Germination was monitored through May 2003, when cages and
remaining seeds were removed from the field. The survivorship of established seedlings
was monitored until August 2003, at which time all seedlings were destroyed.
Linking the Stages
I calculated transition probabilities (TPs) for each stage, from seed removal through
seedling establishment (Rey and Alcantara 2000, Traveset et al. 2003). The first two TPs
are based on observational data from foraging observations collected at adult Sapium
trees in the prairie habitats, while the remaining three TPs come from the experimental
tests conducted in all four habitats. Each TP is the ratio of the number of individuals that
survived a given stage to the number of individuals that entered that stage.
TP1 is the probability that a seed is bird-dispersed, and is calculated as 1-
probability of a seed being dropped. Seeds that were removed from branches and
dropped below the parent tree were assumed no longer available for avian dispersal. The
probability of being dropped is the ratio of the number of seeds dropped: total number of
seeds removed by birds. This makes the assumption that all seeds not dropped are
dispersed by birds. Renne et al. (2000) estimated that approximately 10% of seeds are
dislodged from branches and fall to the ground without being handled by birds. To
estimate this metric for my study trees, I bagged six branches and observed a comparable
abscission rate to that of Renne et al. (2000). I also observed bill marks on nearly all
seeds found on the ground, evidence of removal by birds. Therefore, I assumed seeds not
dropped were dispersed because all study trees were depleted of seeds by late February,
when foraging observations were terminated.
TP2 is the probability a seed will be dispersed to a particular habitat, as estimated
from postforaging movement. Seeds may be dispersed away from parent trees if they are
carried or ingested. Because the next perch was not always seen and because seed arrival
could not be confirmed, I simplified postforaging habitats into prairie and forest, and I
assumed that birds stayed in these habitats long enough to defecate or regurgitate seeds.
Thus, the proportion of seeds dispersed to forest sites is the ratio of the number of seeds
ingested + carried in bill to the forest: total number ingested + carried in bill. Likewise,
the proportion of seeds dispersed to prairie sites is the ratio of the number of seeds
ingested + carried in bill to sites within the prairie: total number ingested + carried in bill.
This TP was only calculated for trees close to the forest edge (see above).
TP3 is the ratio of the number of seeds remaining (not predated): the total number
of seeds placed at experimental sites (192 seeds/habitat). TP4 is the ratio of the number
of seeds that germinated: the total number of seeds placed at experimental sites (192
seeds/habitat). Finally, TPS is the ratio of the number of germinated seeds that
successfully established: the total number of seeds that germinated in a given habitat.
Because the calculation of transition probabilities is based on bird-dispersal, data from
water soaked seeds were not used. The overall or cumulative probability of recruitment
in a particular habitat is the product of the TPs for that habitat. The goal is to compare
among habitats the probability that a seed will become an established seedling.
Data frequently met neither assumptions of normality nor equal variance, and thus I
relied primarily on nonparametric statistical tests. Because only close trees were used in
the calculation of TP2 (dispersal), I wanted to verify that avian foraging activity at close
trees was comparable to that at far trees. Thus, differences between close and far trees
with respect to the number of seeds dispersed, number of visits, and duration of visits by
the ten most effective dispersers of Sapium were compared using a Mann-Whitney
U-test. This test was also used to compare point count detections of these same ten
species in oak hammock and mixed pine-hardwood to look for differences between these
habitats that might reflect differences in seed arrival. Equation 2-1 shows the Jaccard
index of community similarity, which was used to compare disperser diversity of these
C = (2-1)
where j is the number of species common to sites a and b, a is the number of species in
site a and b is the number of species in site b (Nur et al. 1999).
The proportions of seeds that survived the seed predation experiment were
compared among habitats using 1-way ANOVA of angular transformed data. Tukey's
multiple comparison procedure was used to separate habitats when a significant habitat
effect was found. To compare the proportion of seeds that germinated, I used a Kruskal-
Wallis test, followed by the Nemenyi multiple comparison procedure to separate habitats
(Zar 1999). Seedling establishment, however, only occurred in the two prairie habitats,
which were compared using a Mann-Whitney U-test. The effect of seed treatment (acid
vs. water) on the establishment of seedlings in paired field experiments where
germination occurred (open and shaded wet prairie combined) was analyzed with a
Wilcoxon signed-rank test. Because successful establishment was rare, I compared the
overall probability of recruitment through germination rather than through establishment
using a Kruskal-Wallis test, with habitat groups separated with the Nemenyi multiple
comparison procedure. For statistical analyses l used SPSS 10.0 (SPSS Inc., Chicago,
IL) and Minitab 12.0 (Minitab Inc., State College, PA). All means are reported & SD,
with a = 0.05.
Avian Seed Dispersal
A list of 25 bird species that visited study trees and utilized Sapium seeds as a food
source is given in Table 2-1, with the ten most effective dispersers of Sapium (based on
the number of seeds ingested or carried) highlighted in bold. An additional eight species
visited study trees, but had no interaction with Sapium seeds. Of the 33 species total that
visited trees, 21 species (64%) were observed ingesting or carrying seeds. Dumetella
carolmnensis ingested or carried 333 seeds, more than any other species. However,
D. carolinensis often dropped into thick vegetation below parent trees after foraging, and
is therefore less likely to disperse seeds into adjacent forest habitats. Woodpeckers
(Picidae), on the other hand, made up 40% of the most effective disperser species, and
were frequently seen making long flights into the forest from prairie trees. In addition,
woodpeckers consumed more seeds per visit than any other taxon of birds (Table 2-1).
Calrdinalis cardinalis was ranked as one of the top ten dispersers, primarily because it
made more visits and spent more time in trees than any other species. While this species
did carry and ingest seeds, most seeds removed by it were dropped below parent trees
after the aril was scraped off. Of the seeds removed from branches by birds, 19.8% were
dropped below parent trees, leaving 80.2% of the seed crop available for dispersal. Of
these remaining seeds, 34% were carried to other sites within the prairie, while 66% were
carried to the forest.
Several differences were evident between trees close to the forest edge (< 10 m),
and those far from the edge (> 100 m). Among the ten most effective seed dispersers,
significantly more seeds were ingested or carried from close trees (x = 64.8 & 46.2) than
from far trees (x = 39. 1 & 68.8; U= 137.0, P = 0.017). This difference can largely be
attributed to the woodpeckers, all of which were more common at close trees (Table 2-1).
However, the number of visits/h and amount of time (minutes/h) spent in close verses far
trees did not significantly differ when all ten species were considered together
(U= 117.0, P = 0.385 and U= 123.0, P = 0.186 respectively).
A total of 17 frugivorous bird species that ingested or carried seeds at prairie trees
were detected on point counts in oak hammock and mixed pine-hardwood (Table 2-2).
This represents 81% of the frugivores that visited prairie trees and dispersed seeds. The
Jaccard index of community similarity = C, (which ranges from 0 to 1.0) was high (0.88),
indicating that most of these frugivores occurred in both oak hammock and mixed pine-
hardwood. In addition, all ten of the most effective dispersers of Sapium were detected in
both oak hammock and mixed pine-hardwood (Table 2-2), and the mean number of
individuals detected/point/visit did not significantly differ between these two habitats
(U = 1 17.5, P = 0.364). M~elan2epes carolinus was the most common of these ten species
in both habitats, being detected at all point stations with an average of 1.06
birds/point/visit in oak hammock.
Seed survival in the prairie habitats was distinctly different from the forest habitats
(Figure 2-1). Seeds were rapidly consumed in the prairie habitats during the first ten days
after placement, whereas seeds in the forest habitats were subj ected to lower levels of
predation. The proportion of seeds remaining at the end of the experiment (55 days) was
significantly different among habitats (F3,44 = 13.65, P < 0.001), with 28% and 39%
remaining in shaded and open wet prairie respectively, verses 85% and 79% remaining in
mixed pine-hardwood and oak hammock. The two prairie habitats were significantly
different from the two forest habitats, but open wet prairie was not significantly different
from shaded wet prairie, nor was oak hammock significantly different from mixed
pine-hardwood. Most predation occurred soon after the experiment began, with little
additional seed-predation in any of the four habitats after 20 days. Evidence of
mammalian seed-predation (broken seed coats) was found at experimental sites where
seeds had been placed.
Seed Germination and Establishment
Only one of 192 seeds germinated in mixed pine-hardwood, and seeds failed to
germinate altogether in oak hammock. The highest level of germination success was
observed for water-soaked seeds in shaded wet prairie (65.4%), followed closely by
water-soaked seeds in open wet prairie (60.6%). This was significantly higher than
acid-treated seeds in shaded wet prairie (19.4%) and open wet prairie (9.6%), (H = 53.79,
df = 5, P < 0.001; Chapter 1). The relatively low germination success of acid-treated
seeds in open wet prairie made this habitat statistically indistinguishable from oak
hammock and mixed pine-hardwood, and from acid-treated seeds in shaded wet prairie
Successful germination was no guarantee of successful establishment. Pooling the
results for acid-treated and water-soaked seeds, only about 10% of seeds that germinated
also established. The difference between shaded and open wet prairie was not
significant, SWP = 0.098 & 0. 146 vs. OWP = 0. 111 & 0.269 (U= 318.0, P = 0.335). For
sites in the two prairie habitats where both acid-treated and water-soaked seeds
germinated, a slightly higher proportion of water-soaked seeds established (mean = 0. 12
& 0.16) than acid-treated seeds (mean = 0.09 & 0.25). However, this difference was not
significant (T = -1.173, P = 0.241). In both open and shaded wet prairie, newly
germinated seeds were frequently attacked by fire ants (Solenopsis invicta) soon after the
seed coat had split, thus preventing seedling establishment. In addition, some seeds
germinated in moist microsites that subsequently desiccated shortly after the seeds
germinated. These seeds rarely survived long enough to become established seedlings.
Linking the Stages
Multiplying the process-specific transition probabilities (TPs) pooled across all 12
sites within each habitat resulted in an overall probability of recruitment through the
seedling stage of 0.001 in both prairie habitats, and zero in the two forest habitats
(Figure 2-3). With each site considered an independent replicate, there was a significant
difference among habitats in the overall probability of becoming a germinated seed
(H = 1 1.26, df = 3, P = 0.01). Pooled across all sites within each habitat, the overall
probability of becoming a germinated seed was 0.010 and 0.015 in open and shaded wet
prairie respectively, verses 0.003 and zero in mixed pine-hardwood and oak hammock.
However, relatively low germination success in open wet prairie made this habitat
statistically indistinguishable from oak hammock and mixed pine-hardwood. Only in
shaded wet prairie was there a significantly higher probability of becoming a germinated
Establishment probability may be determined by dispersal or by postdispersal
processes. In this study, dispersal limitation is unlikely to explain the absence of Sapium
in oak hammock or mixed pine-hardwood. This conclusion is supported by the
observation that 66% of seeds taken by birds at close trees were moved in the direction of
the forest habitats, and all ten of the most effective dispersers of Sapium were detected on
point counts in the two forest habitats. I am unable to confirm if the individuals detected
on point counts also foraged at Sapium trees in the adj acent prairie habitats. Seed traps
were not used in the forest due to the infinite number of perch sites below which seed
deposition might occur. However, the frequent movement of seeds into forest habitats
combined with the abundance of these species in the forest strongly suggests that seed
arrival is taking place. This underscores the importance of examining multiple stages in
the recruitment process, and then linking these stages to determine which if any is
responsible for limiting recruitment at a given site. At this site, I showed that
germination is the stage most likely responsible for preventing recruitment in the forest
Avian Frugivory and Seed Dispersal
This is the first study to examine avian frugivore activity at Sapium in Florida, yet
close parallels exist with respect to species richness and foraging behavior from sites in
South Carolina, Louisiana, and Texas. In South Carolina, Renne et al. (2000, 2002) also
found woodpeckers to be among the most common dispersers of Sapium seeds.
However, they also found Sturnus vulgaris, Corvus ossifragus, and Quiscalus major to be
potentially important dispersers, largely because they arrived in flocks that collectively
consumed many seeds. In this study, not only did these species not visit Sapium trees,
but flocks of birds were rarely observed. If flocks visited study trees outside of
observation periods, one would expect large variation in removal rates from day to day. I
marked eight branches on four trees, and instead observed a gradual loss of seeds over the
winter (Samuels, unpublished). This confirms that flocks did not commonly visit study
trees outside of observations, and that foraging data accurately represent frugivore
activity at Sapium trees through the winter of 2002-03. It is unknown why flocks were
virtually absent at this site, but it may relate to the low density of Sapium trees due to past
I observed Calrdinalis cardinalis dropping more seeds below parent trees than any
other species, an observation that agrees with Renne et al. (2000, 2002). Dropping of
seeds usually was preceded by scraping, where the bill is used to scrape the aril off the
seed without ingesting the seed. However, Conway et al. (2002a) never observed
C. cardinalis scraping seeds at a site in Texas. Furthermore, they found Icterus galbula
to be frequent consumers of Sapium seeds that never scraped seeds. In the present study,
L. galbula never ingested seeds, but readily scraped them to consume the aril.
The 21 bird species observed ingesting or carrying Sapium seeds belong to eight
families with a diversity of foraging strategies. This supports the view that generalized
dispersal syndromes common to vertebrate-dispersed plants have aided the invasion
process of exotic plants that posses these traits (Richardson et al. 2000). Introduced
species may account for as much as one-third of the bird-dispersed flora in eastern North
America (White and Stiles 1992), and the presence of fruits during winter when insect
availability is low may further increase the use of these resources at least in the southeast
USA (Skeate 1987, McCarty et al. 2002). Avian dispersal of exotic seeds then leads to
the formation of satellite populations, although it remains unclear how land-use and
landscape connectivity affect the movement of invasive species into natural areas
(Reichard et al. 2001). Dispersers of Sapium at this site readily crossed abrupt habitat
boundaries, insuring that seeds arrived in a wide diversity of microsites. Successful
invasion of new locations at this site is most likely to depend on postdispersal processes.
Postdispersal seed-predation varied among habitats, but the survival of seeds was
similar between the two prairie habitats, and likewise between the two forest habitats.
The level of predation was significantly higher in the prairie habitats where Sapium
presently occurs, thus postdispersal seed-predation cannot solely explain the failure of
Sapium to establish in the forest habitats at this site. The lower level of seed loss in the
forest habitats may be due to a lower species richness or abundance of seed predators.
Through preliminary investigations, I obtained photos of marsh rabbit (Sylvilagus
palustris), eastern cottontail (Sylvilagus florid~dd~~dd anus), and rice rat (Oryzomys palustris)
consuming Sapium seeds in the prairie habitats, but no photos were obtained of
seed-predators in the forest. The open understory and tall tree canopy in the forest
habitats may increase the risk of predation to mammalian seed-predators relative to the
prairie habitats where cover is present near the ground. The extent of cover can alter the
foraging behavior and habitat selection of potential seed-predators (Lima and Dill 1990,
Bowers and Dooley 1993). Alternatively, the deep litter present in the forest habitats
may have succeeded in sheltering seeds from potential predators. Thick litter has been
shown to hinder the detection of seeds by rodents (Cintra 1997).
Mammals (especially rodents) are well known to be important seed-predators in
temperate ecosystems (Mittelbach and Gross 1984, Hulme 1998, Hulme and Hunt 1999,
Anderson and MacMahon 2001, Maron and Simms 2001), and there is no evidence that
exotic species are less susceptible than native species to seed-predation (Blaney and
Kotanen 2001). Seed burial reduces postdispersal predation, and it is likely some Sapium
seeds would enter the seed bank following avian dispersal. Renne et al.(2001) found that
Sapium seeds buried for one and two years did not differ in viability. Furthermore,
Cameron et al. (2000) suggest that seeds may be viable for up to seven years.
Extrapolation of surface seed-predation data to the dynamics of plant recruitment should
therefore proceed with caution (Hulme 1994).
The nearly complete lack of germination in the two forest habitats suggests that
germination is a strong barrier to recruitment, and is preventing establishment of Sapium
in oak hammock and mixed pine-hardwood forests at Paynes Prairie. Placement of seeds
on top of the litter layer, which was meant to simulate the state of recently dispersed
seeds, may have inhibited germination by preventing contact with a moist soil substrate.
Seeds that were suspended in litter were always dry when sites were checked for signs of
germination, and litter appeared to dry out quickly after rains. It is thus not surprising
that the only seed that germinated in mixed pine-hardwood forest was at a site where
water had pooled after heavy rain, and conditions were appropriate for imbibition to
occur. Soaking of Sapium seeds in water has been suggested as a process that initiates
germination (Conway et al. 2000).
Alternatively, seeds may have failed to germinate in the forest habitats because of
reduced variation in daily temperature fluctuations. Fluctuating temperatures have been
shown to increase germination success of Sapium (Nijj er et al. 2002), and forest habitats
may buffer microsites against large fluctuations. This hypothesis is unlikely, however,
because seeds also failed to germinate in a shade-house that simulated the forest floor
environment, and temperature fluctuations were consistent among treatments that
included high levels of germination (Samuels, unpublished).
The presence of a thick litter layer in forest habitats at Paynes Prairie is partly a
result of fire suppression near residential areas. Reduction of litter through fire or
through manual removal can alter microsites to create favorable conditions for
germination (Carrington 1999, McConnell and Menges 2002), introducing the possibility
that a fire in the forested habitats at the Paynes Prairie site might create suitable sites for
Sapium establishment if seeds arrived. In contrast, Renne (2001) found Sapium invading
mixed pine-hardwood and other forest habitats at a site in South Carolina where
prescribed burns are common. In a field plot study, Renne (2001) observed over 40%
emergence of sown seeds in mixed pine-hardwood. Plots had been cleared of litter and
vegetation to standardize treatments, and seeds were sown 0.5 cm deep. Both of these
factors likely contributed to the large differences in germination success between that
study and the present study; burial likely increased the chance that seeds would be
surrounded by moisture. In comparison, Siemann and Rogers (2003) added Sapium seeds
to the surface of a mesic forest in Texas dominated by pines and oaks and observed low
germination success (5-10%) and 100% seedling mortality. Thus, if seeds had
germinated and established in oak hammock and mixed pine-hardwood forests in the
present study, seedling mortality may still have prevented the recruitment of adult plants
in these habitats.
Recruitment Limitation in Forest Habitats
The outcome of any one stage alone cannot be used to predict recruitment patterns
because of independence among processes acting at different stages (uncoupling), and
because patterns of uncoupling among stages are site-specific (spatial discordance;
Jordano and Herrera 1995). Thus, uncoupling between consecutive stages within a site or
spatial discordance in the probability of seed survival, germination, or establishment
among sites can obscure the importance of any particular stage when considered in
isolation (Herrera et al. 1994, Jordano and Herrera 1995, Houle 1998). However, the
relative importance of each stage in the recruitment process can be evaluated through an
experimental framework where seed dispersal is monitored or manipulated through seed
sowing experiments, and the fate of a cohort of propagules is followed through each stage
(Schupp and Fuentes 1995, Nathan and Muller-Landau 2000, Garcia 2001, Banack et al.
2002, Balcomb and Chapman 2003). Using this general framework, I was able to
identify germination as the limiting stage, or the "Achilles heel" in the process of
seedling recruitment in oak hammock and mixed pine-hardwood. Recruitment following
seed introduction indicates the presence of a regeneration niche, and a lack of recruitment
may indicate that suitable microsites were absent at the time of seed sowing (Turnbull et
al. 2000). However, suitable microsites for seedling establishment still do not guarantee
that plants will survive to become reproductive adults, which is required to satisfy the
assumption that existing seed shadows ultimately translate into self-reproducing
populations (Schupp and Fuentes 1995).
By calculating transition probabilities among stages, I was able to detect both
uncoupling between successive stages within habitats, as well as spatial discordance of
particular stages among habitats. High spatial discordance has been detected in other
studies using similar research designs. Rey and Alcantara (2000) found that seedling
survival was the most critical process during recruitment of Olea europaea (Oleaceae),
with the most favorable places for seeds becoming the worst places for seedlings.
Traveset et al. (2003) found both seedling survival and postdispersal seed-predation to be
critical stages for Rhamnnus ludovici-salvatoris (Rhamnaceae), with high spatial
discordance among habitats. In both studies, water stress was identified as the principal
reason seedlings failed to survive, with low precipitation also contributing to low
germination (Traveset et al. 2003). In the present study, spatial discordance occurred
among habitats for the germination stage, imposing an abrupt contrast between forest and
prairie habitats with respect to this stage. Because germination was virtually absent in
the forest habitats, this stage obscured the relative importance of earlier stages in the
recruitment process. It remains unknown whether seedlings could have established in
oak hammock and mixed pine-hardwood had they germinated in these habitats.
Estimates of transition probabilities in this study are constrained by the short, one
year, duration of the study. There has been growing interest in how the effects of
variation in the physical environment interact with biology to produce patterns seen in
nature (Chesson 2003). Seedling recruitment and survival vary considerably from year to
year both within and among populations, and one year' s results cannot be used as reliable
long-term estimates of these parameters (Clark et al. 1999, Ibafiez and Schupp 2001).
However, germination was such a formidable barrier to recruitment in the forest habitats
that this parameter seems unlikely to increase substantially unless some form of
litter-reducing disturbance is imposed. Annual fluctuations in temperature and
precipitation are unlikely to create favorable regeneration niches in the forest habitats,
although such variation could easily alter the extent of recruitment success in the prairie
Assessing recruitment limitation in the forest habitats relied upon the assumption
that observational data of avian foraging behavior can be tied to experimental data of
postdispersal processes. The overall probability of recruitment explicitly includes both
forms of data as the product of all transition probabilities, where TP1 and TP2 are derived
from observational data, while all remaining transition probabilities come from
experimental data (Figure 2-3). However, the probability of a seed being dispersed to
forest vs. prairie habitats is based on observation only of the three trees close to the forest
edge. This may explain why 66% of seeds were dispersed to forest habitats. Sapium
trees near the edge were visited by many woodpeckers that likely came from and returned
to the forest. However, the percent of seeds dispersed to prairie habitats (34%) is likely
an underestimate, since most seeds dispersed away from trees more distant in the prairie
are more likely to arrive within prairie habitats. In addition, seeds dropped below parent
trees arrive in the prairie habitats, even if they are not dispersed. To evaluate the
potential impact of this bias, I let TP1 and TP2 = 1.0, while all other TPs were held
constant. This resulted in an overall probability of recruitment of 0.004 and 0.003 for
shaded and open wet prairie respectively, compared to 0.001 for both prairie habitats
when TP1 = 0.802 and TP2 = 0.340 (Figure 2-3). Thus, variance in these parameters does
not have a large effect on the overall probability of becoming a seedling. Alternatively,
TP2 (dispersal) may be an overestimate for the forest habitats. However, the overall
probability of recruitment goes to zero regardless of the probability of dispersal because
germination was the limiting stage.
The long-term forecast for Sapium invasion at Paynes Prairie Preserve State Park
and other natural areas in north Florida may depend on future management activities that
create or remove appropriate microsites for establishment. For now, Sapium is absent
from oak hammock, mixed pine-hardwood forest, and other upland mixed hardwood
forests. Results from the present study suggest that postdispersal processes are limiting
the current extent of invasion, but that seeds may be present to take advantage of
regeneration niches if or when they become available. Control efforts continue at Paynes
Prairie within the prairie habitats themselves, although outright eradication appears
remote due to the inaccessibility of some trees, rapid maturation of new recruits, and
continued arrival of seeds via local waterways and birds. Paynes Prairie and other natural
areas will continue to be at risk from seed input originating from ornamental trees still
present in local residential areas. While efforts to increase awareness of this species have
been somewhat successful (Putz et al. 1999), source trees are likely to be present for
some time to come.
Table 2-1. Bird species seen visiting six Sapium sebiferum trees during 106.5 hours of observation between 6 October 2002 and 25
February 2003, Paynes Prairie Preserve State Park, Alachua County, FL.
Species Status" Ingested Seeds Dropped Seeds Carried Seeds Visits/hr to Trees Min/hr in Trees
Near Far Near Far Near Far Near Far Near Far
Melanerpes carolinus I,D,C 12 12 1 1 47 1 0.35 0.08 0.61 0.09
Picoides pubescens I,D,C,S 10 11 1 0 14 12 0.50 0.44 0.81 0.45
Colaptes auratus I,D,C 171 23 1 2 1 0 0.17 0.10 0.48 0.29
Dryocopus pileatus I 91 0 0 0 0 0 0.09 0 0.19 0
Sayornis phoebe I,D,C 54 23 1 1 4 0 0.62 0.38 0.86 0.59
Myiarchus cinerascens* I 13 0 0 0 0 0 0.07 0 0.17 0
Cyanocitta cristata I,D,C,S 1 3 2 0 1 2 0.37 0.19 0.28 0.22
Regulus calendula P 0 0 0 0 0 0 0.15 0.06 0.15 0.05
Catharus guttatus I,C 7 4 0 0 1 2 0.09 0.06 0.10 0.05
Turdus migratorius I,D 33 12 1 0 0 0 0.24 0.04 0.75 0.12
Dumetella carolinensis I,D,C 96 221 5 17 4 12 2.00 2.12 2.68 3.06
Mimus polyglottos I,D 30 25 1 0 0 0 0.37 0.52 0.76 1.28
Toxostoma rufum I 0 9 0 0 0 0 0 0.12 0 0.07
Vireo griseus I,D,C 22 4 1 0 0 3 0.39 0.19 0.36 0.20
Vireo solitarius I,D 4 1 1 0 0 0 0.11 0.02 0.13 0.02
Vireo olivaceus I 0 1 0 0 0 0 0 0.02 0 0.02
Vermivora celata P 0 0 0 0 0 0 0.13 0.04 0.10 0.04
Dendroica pinus D,C,P 0 0 1 0 2 0 0.09 0.02 0.10 0.01
Dendroica coronata D,C,S,P 0 0 0 3 1 2 1.49 1.83 2.94 4.43
Cardinalis cardinalis I,D,C,S 36 24 115 107 23 8 2.77 1.37 4.07 2.13
Passerina cyanea C 0 0 0 0 0 1 0.02 0.02 0.04 0.01
Agelaius phoeniceus I 0 1 0 0 0 0 0 0.08 0 0.15
Quiscalus quiscula I 1 0 0 0 0 0 0.15 0.02 0.15 0.04
Icterus galbula D,S,P 0 0 0 5 0 0 0.17 0.13 0.21 0.23
Carduelis tristis S 0 0 0 0 0 0 0.07 0 0.05 0
Total: 581 374 131 136 98 43 10.46 8.06 16.00 13.72
For each species, the number of seeds ingested, dropped,
Species in bold are the ten most effective dispersers of Sapium at this site.
and carried is given along with the amount of time spent in observation trel
a Frugivory status of birds at Sapium sebiferum, Paynes Prairie Preserve State Park, Alachua County, Florida. I = ingested seeds, D
= dropped seeds after removing from branch, C = carried seeds away from tree, S = scraped aril off seeds, P = pecked at aril on
* Out of range species.
Table 2-2. Frugivorous bird species detected on point counts in oak hammock and mixed
pine-hardwood habitats between 12 October 2002 and 5 March 2003, Paynes
Prairie Preserve State Park, Alachua County, FL.
Oak Hammock Mixed Pine-Hardwood %
Mean (SD)b % (50-m)" Mean (SD)b % (50-m)" (Total)d
Melanerpes carolinus I,C,D 1.06 (0.24) 100.0 0.75 (0.35) 100.0 100.0
Picoides pubescens I,C,D,S 0.23 (0.21) 83.3 0.26 (0.12) 100.0 91.3
Colaptes auratus I 0.05 (0.07) 33.3 0.14 (0.13) 63.6 47.8
Dryocopus pileatus I 0.04 (0.09) 16.7 0.06 (0.13) 27.3 21.7
Sayornis phoebe I,C 0.14 (0.16) 66.7 0.05 (0.10) 27.3 47.8
Vireo olivacerts I 0 0 0.03 (0.09) 9.1 4.3
Vireo griseus I 0.27 (0.27) 75.0 0.04 (0.07) 27.3 52.2
Vireo solitaritis I 0.01 (0.04) 8.3 0.08 (0.10) 45.5 26.1
Cvanocitta cristata SC 0.65 (0.30) 100 0.25 (0.31) 63.6 82.6
Turdus migratorius I 0.08 (0.10) 50.0 0.38 (0.88) 63.6 56.5
Cathartis grittatus I,C 0.14 (0.19) 50.0 0.06 (0.10) 36.4 43.5
Dumetella carolinensis I,C,D 0.29 (0.34) 66.7 0.03 (0.06) 18.2 43.5
Mimus polyglottos I 0.17 (0.19) 50.0 0.03 (0.09) 9.1 30.4
Toxostoma rufum I 0.11 (0.12) 58.3 0.03 (0.06) 18.2 39.1
Dendroica pinus PC 0.06 (0.06) 25.0 0.18 (0.36) 36.4 30.4
Cardinalis cardinalis I,C,D,S 0.81 (0.64) 91.7 0.30 (0.24) 81.8 87.0
Quiscalus quiscula I 0.69 (1.58) 33.3 0 0 17.4
Species in bold represent the ten most effective seed dispersers of Sapium sebiferum
based on foraging observations in adj acent prairie habitats (Table 2-1).
a Frugivory status as in Table 2-1.
b Mean number of individuals detected per 50-m-radius point count per visit (n = 7
visits/point to 12 points in Oak Hammock, and 11 points in Mixed Pine-Hardwood).
" The percentage of 50-m-radius point counts within which the species was detected.
d The percentage of all forest point counts (OH + MPH) within which the species was
S60 -*--~ SWP
u, -e- OWP
50 I-- OH
u, 40 -*- MPH
0 10 20 30 40 50 60
Figure 2-1. Sapium seed survivorship in shaded wet prairie (SWP), open wet prairie
(OWP), oak hammock (OH), and mixed pine-hardwood (MPH) habitats at
Paynes Prairie Preserve State Park, Alachua County, FL. Time 0 = 22
.9 0.4 -1 b
o 0.3 _1 a,b
0.1 aI a
AOH AMPH AOWP ASWP WOWP WSWP
Figure 2-2. Mean proportion of Sapium seeds (+ SD) that germinated. Treatment groups
from left to right include acid treated seeds in oak hammock (AOH), mixed
pine-hardwood (AMPH), open wet prairie (AOWP) and shaded wet prairie
(ASWP). Water soaked treatments were applied to open wet prairie
(WOWP), and shaded wet prairie (WSWP). Treatments with the same letters
above error bars are not significantly different at a = 0.05. Figure modified
from Chapter 1.
S WP O WP IVPH OH
TP1 0.802 0.802 0.802 0.802
TP2 0.340 0.340 0.660 0.660
TP3 0.281 0.391 0.854 0.786
TP4 0.194 0.096 0.006 0
TPj 0.071 0.091 0 0
OPRI 0.001 0.001 0 0
Figure 2-3. Spatial dynamics of recruitment through seedling establishment for Sapium
sebiferum in shaded wet prairie (SWP), open wet prairie (OWP), mixed pine-
hardwood (MPH) and oak hammock (OH). The values in boxes represent
overall process-specific transition probabilities (TPs), the product of which
gives the overall probability of recruitment (OPR) for S. sebiferum in that
habitat. TP1 is the probability that a seed is bird dispersed, TP2 is the
probability of seed dispersal to each of the four habitats, TP3 is the probability
that a dispersed seed is not predated, TP4 is the probability that a seed will
germinate, and TPS is the probability that a germinated seed will establish.
TP1 and TP2 WeTO Obtained through foraging observations at S. sebiferum
trees; all other TPs obtained through experimental data pooled across all 12
sites in that habitat. Diagram based on Figure 2 in Rey and Alcantara (2000).
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Ivan Samuels was born in San Francisco, California, where he developed an
interest in birds and nature at the age of 12. He completed Bachelor of Arts degrees in
biology and environmental studies at the University of California, Santa Cruz in 1998.
After graduating, Ivan pursued numerous field-work opportunities, studying birds in both
temperate and tropical locations, with an emphasis in conservation.