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Spring 5-13-2016

Determining the pollination mechanism of a problematic invasive species in the Gulf South: Triadica sebifera

Jennifer Wester Clark University of New Orleans, [email protected]

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Recommended Citation Clark, Jennifer Wester, "Determining the pollination mechanism of a problematic invasive species in the Gulf South: Triadica sebifera" (2016). University of New Orleans Theses and Dissertations. 2134. https://scholarworks.uno.edu/td/2134

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This Thesis has been accepted for inclusion in University of New Orleans Theses and Dissertations by an authorized administrator of ScholarWorks@UNO. For more information, please contact [email protected]. Determining the pollination mechanism of a problematic invasive species in the Gulf South: Triadica sebifera

A Thesis

Submitted to the Graduate Faculty of the University of New Orleans in partial fulfillment of the requirements for the degree of

Master of Science in Biological Sciences

by

Jennifer Wester Clark

B.S. University of New Orleans, 2011

May 2016

Acknowledgement

I would like to thank my advisor, Dr. Jerome Howard, for his inspiration, advice, and encouragement throughout my project. I would also like to thank my committee members, Dr.

Charles Bell and Dr. Philip DeVries, for their guidance and assistance.

Thank you to Scott Hereford and staff at the Mississippi Sandhill Crane National Wildlife

Refuge and staff at Tulane University’s F. Edward Hebert Riverside Research Center for assisting me when needed. Many thanks to Dr. Mary Clancy for her microscope expertise and to the undergraduate research assistants I had out in the field, Crista, Brittany, and Becky.

Special thanks to my lab mates Cara Nighohossian, Lizzie Ruffman, and Robinson Sudan, and fellow graduate students Lauren Gonzalez, Catie Policastro, and Trent Santonastaso for all of their knowledge and encouragement.

Lastly, thank you to my wonderful family for their love and encouragement, especially my husband for his support and patience.

ii Table of Contents

List of Figures ...... iv List of Tables ...... v Abstract ...... vi Introduction ...... 1 Invasive Species ...... 1 Triadica sebifera characteristics ...... 2 Triadica sebifera as an invasive species in the U.S...... 4 Methods...... 7 Study sites ...... 7 Sampling design ...... 9 Self-fertilization survey ...... 9 Receptivity survey ...... 10 Airborne pollen count ...... 11 Insect pollination survey ...... 11 Insect identification ...... 12 Pollen identification ...... 12 Statistical analysis ...... 12 Results ...... 14 Self-fertilization survey ...... 14 Receptivity survey ...... 14 Airborne pollen count ...... 15 Insect pollination survey and identification ...... 16 Pollen identification ...... 18 Discussion ...... 19 References ...... 22 Appendix ...... 30 Receptivity Data...... 30 Insect Identification ...... 30 Vita ...... 34

iii

List of Figures

Figure 1: Range of T. sebifera in the U.S...... 4

Figure 2: Map of Tulane University's F. Edward Hebert Riverside Research Center ...... 8

Figure 3: Map of Mississippi Sandhill Crane National Wildlife Refuge...... 9

Figure 4: Bagged inflorescence ...... 10

Figure 5: Tagged inflorescence post- exposure ...... 11

Figure 6: Pollen trap...... 11

Figure 7: Pollen grains vs. distance from source tree ...... 16

iv List of Tables

Table 1: Proportion of fruits developed per test tree in self-fertilization survey ...... 14

Table 2: Repeated measured ANOVA of fruit set among trees over time ...... 15

Table 3: Number of pollen grains per microscope field for two trees at varying distances ...... 15

Table 4: Comparison of abundance of taxa visiting at two sites...... 17

Table 5: Species diversity by order and bee family at both sites ...... 18

Table 6: Mean and standard deviation of 5 field views of pollen loads per group ...... 18

Table 7: Numbers of fruits developed in receptivity exclusion experiment ...... 30

Table 8: Arthropods collected (ms stands for morphospecies) ...... 30

v Abstract

Understanding the ecology of invasive species is vital to curb the homogenizing of ecosystems, yet the pollination mechanisms of the Chinese tallow tree (Triadica sebifera) in its introduced habitat remain ambiguous. This study examines self-pollination, wind pollination, and flower- visiting insects of tallow in a bottomland hardwood forest and Longleaf pine savannah in the U.S.

Gulf South. These data suggest that self-pollination and airborne pollination are possible, but likely rare occurrences, although the possibility of apoxisis was not investigated. Seed production in exclusion experiments was significantly less than in open-pollinated flowers, and wind dispersal of tallow pollen dropped to essentially zero 8 meters from the source. Results show that tallow is primarily bee pollinated, with external pollen loads of Apis, Melissodes, and halictids visiting at similar rates, and Xylocopa species visiting less frequently. The researchers believe that to date, this is the first study of the pollination mechanisms of T. sebifera in its introduced range and recommend further study to understand the ecology of this destructive invasive species.

Triadica sebifera, Chinese tallow, invasive species, pollination, arthropods, Longleaf pine savannah, bottomland hardwood forest

vi Introduction

Invasive Species

It has been known for decades that invasive species have negative effects on native species, communities, and ecosystems (Elton 1958, Simberloff 1996). Invasive species are found in almost every habitat on earth (Mack et al. 2000) and considered second only to habitat loss and fragmentation as a threat to global biodiversity (Sakai et al. 2001, Walker and Steffen 1997).

Not only do invasive species alter ecosystem structure and processes, reduce native diversity, and contribute to extinction of native organisms (Cleland et al. 2004, Mack et al. 2000, Mooney and Hobbs 2000, Wilcove et al. 1998), but they also have significant economic impacts, costing over $120 billion annually (Pimentel et al. 2005).

Human activity is a major cause of long-distance introductions of nonindigenous species.

Exotic flora has been introduced into new areas for ornamentation, agriculture, and erosion control, amongst other reasons (Wilcove et al. 1998). In the U.S. alone, an estimated 5,000 invasive species introduced for agricultural, textile, and horticultural purposes have escaped domestication (Morse et al. 1995).

For many introduced species, biotic interactions rather than the physical environment may determine the persistence of introduced populations, the degree to which they become invasive, and the geographic distribution in the introduced range. While competition from native species and escape from natural enemies has been investigated in many systems (Levine et al.

2004, Maron and Vila 2001, Mitchell and Power 2003), until recently mutualistic interactions facilitating the spread of invasive species has received less attention. Mutualistic interactions involving both pollination and seed dispersal appear to be common and important factors in the

1 success of invasive plant species (Richardson et al. 2000). In most cases there appears to be adequate service to introduced species by generalist mutualists to permit successful establishment and spread. However, this does not appear to always be the case.

In some habitats, non-native pollinators more closely associate with non-native plant species (Morales and Aizen 2006). Studies in Argentina, Australia, Canada, and New Zealand demonstrated the existence of invasive pollination mutualisms, where introduced bees visit exotic plant species over native flora (Donovan 1980, Morales and Aizen 2006, Pearson and

Braiden 1990, Stimec et al. 1997, Woodward 1996). In some cases, invasive mutualisms between introduced plants and pollinators appear to be a crucial factor in the establishment and spread of invasive plant species. In North America, introduced honeybees (Apis mellifera) are the main pollinators of two important non-native weeds, purple loosestrife (Lythrum salicaria, Mai et al.

1992), and wild radish (Raphanus sativus, Stanton 1987), and have been shown to increase seed set of yellow star thistle (Centaurea solstitialis, Barthell et al. 2001). The role of mutualisms in the establishment and spread of invasive plant species deserves greater attention.

Triadica sebifera characteristics

Triadica sebifera, commonly known as the Chinese tallow tree, popcorn tree, Florida aspen, and chicken tree, belongs to the large and diverse family Euphorbiaceae (Jubinsky and

Anderson 1996). Chinese tallow is a subtropical, deciduous tree. Its flowers are monoecious, and the tree is polycarpic. The tree has greyish-brown fissured bark and exhibits plasticity in growth form, ranging from shrubby with lateral branches to tall trees with pendent branches (Jubinsky and Anderson 1996). It can grow to heights of 10 to 15 meters (Bruce et al. 1997, Duke 1983).

Leaves are alternately whorled and distinctively heart-shaped with blades 5-8 cm long and 4-6 cm wide. They are dark green with light green veins and turn yellow to red in the fall.

2 Flowers are yellow-green in terminal spike-like inflorescences 5-20 cm long. Staminate flowers are in clusters along the spike. Pistillate flowers are clustered at the base of the spike and are reduced with a three-lobed ovary, three styles, and no petals. Trilocular capsule fruits are 9-19 mm across and split to reveal three white, wax-coated seeds 6-10 mm in diameter that remain attached until winter (Bogler 2000, McCormick 2005, Meyer 2011, Miller 2003).

Chinese tallow exhibits r-strategist life history traits. Generation time is short, with maturity reached in as little as three years (Duke 1983, Scheld et al. 1984). Fecundity is high due to prolific seed production (Renne et al. 2000, Scheld and Cowles 1981). A mature stand of trees can produce seeds in excess of 4,500 kg per acre per year (Conway et al. 2000), and trees remain sexually viable to 60 years (USGS/NWRC 2000). Growth is rapid (Lin et al. 2004) and is equal or greater than numerous native seedlings in most conditions (Jones and McLeod 1989, 1990).

Trees reach a maximum height of 10-15 meters in 10-12 years (Duke 1983). Other r-selected traits of Chinese tallow include widespread seed dispersal by birds and moving water (Jubinsky

1995, McCormick 2005, Meyer 2011, Renne et al. 2002), and its ability to survive in disturbed and unstable environments (Jubinsky 1995, McCormick 2005, Meyer 2011).

Chinese tallow is native to southeastern China and Japan. It has been introduced to the

Korean Peninsula, Vietnam, Singapore, Sri Lanka, India, Sudan, South Africa, Algeria, Italy,

France, Brazil, Martinique, Jamaica, Cuba, Mexico, and the U.S. (Duke 1983, ISSG 2005,

McCormick 2005). Its range in the U.S. extends from North Carolina south to Florida, west into

Texas, and north to Oklahoma, Arkansas, Tennessee, and Kentucky. It has also been found in

Wisconsin, California, and Hawaii (Fig. 1) (CISEH 2010, McCormick 2005, Siemann and

Rogers 2003).

3

Figure 1: Range of T. sebifera in the contiguous U.S.

Triadica sebifera as an invasive species in the U.S.

The first documentation of the intentional introduction of Chinese tallow to the U.S. is in a letter from Benjamin Franklin in 1772. Franklin, while visiting Asia, sent a few seeds to his friend and gentleman farmer, Noble Wimberly Jones, in Darien, Georgia (Bell 1966). The first botanical reference to the plant in the U.S. was in 1803 by Andreas Michaux, who observed its cultivation in Charleston, South Carolina and Savannah, Georgia, and noted its unaided spread into coastal forests (McCormick 2005). In 1906, Chinese tallow was brought to Texas and

Louisiana by the USDA’s Foreign Plant Introduction Division to establish a commercial soap industry (Flack and Furrow 1996, Siemann and Rogers 2001). It is favored in the horticulture industry as an ornamental due to its fall foliage (Maddox et al. [date unknown], McCormick

2005).

Since its introduction to the U.S., Chinese tallow has aggressively displaced native flora and formed monospecific stands. It can invade both intact and disturbed habitats (Conner et al. 2002,

Neyland and Meyer 1997, Varner and Kush 2004). Chinese tallow readily invades grassland communities and does especially well in coastal prairies, where it has been shown to convert to closed-canopy forests within 10 years of establishment (Bruce et al. 1995, Grace 1998, Meyer

2011). It invades numerous woodland habitats, including bottomland hardwood, pine, floodplain,

4

riparian, and mixed (Harcombe et al. 1998, Ramsey et al. 2005, Renne et al. 2000, Varner and

Kush 2004), and is successful in wet habitats, along lake and river shores, in floodplains, and in wetlands, including floating marsh thickets (Bruce et al. 1997, Meyer 2011, Miller 2003, Nolfo-

Clements 2006). It invades disturbed sites such as agricultural lands, roadsides, spoilbanks, storm-damaged habitats, utility rights-of-way, and urban areas (Loewenstein and Loewenstein

2005, Maddox et al. [date unknown], Mann 2006, Ramsey et al. 2005, Varner and Kush 2004).

The competitive dominance of Chinese tallow is due to multiple factors, including its r- strategist life history traits. These traits include rapid growth, high fecundity, short generation time, generalized avian seed dispersal, and tolerance to a wide range of environmental conditions, including acid to alkaline soils, wet to droughty landscapes, deep shade to full sun, and saline to freshwater flooding (Conner et al. 1997, McCormick 2005, Meyer 2011). Adding to its success is a low herbivore load in its introduced range (Bruce et al. 1997), and the ease at which roots develop shoots and stumps resprout (Urbatsch 2000).

Understanding the ecology of invasive species is vital to curbing impacts on native species and the homogenization of ecosystems (Mack at al. 2000, Sakai et al. 2001). Despite the threats that Chinese tallow poses, some characteristics of this invasive plant remain unknown.

Surprisingly, the mechanisms of pollination of this plant in its introduced habitat remain ambiguous (Meyer 2011). A fact sheet produced by the University of Georgia’s Center for

Invasive Species and Ecosystem Health states that Chinese tallow is wind pollinated (Evans et al.

2006). While this is generally consistent with the tendency of the Euphorbiaceae to produce spicate inflorescences containing many reduced flowers, entomophily is common in the family and consistent with this floral morphology (Webster 1994). The United States Department of

Agriculture notes Chinese tallow being used by beekeepers (Miller 2003), and was apparently

5 aggressively planted throughout the Gulf Coast as a nectar source for honeybees and the quality of its honey (Hayes 1979). The close association between Chinese tallow and the introduced honeybee may comprise an invasive mutualism that could have been important to the spread of tallow in North America, but there is no information on tallow visitation by native or introduced pollinators. The pollination mechanisms of Chinese tallow have not been explored in sufficient detail to determine the dominant mode of pollination and whether this may influence its success as an introduced species. In this study I aim to evaluate pollination mechanisms in Chinese tallow on the central Gulf Coast.

6 Methods

Study sites

The study was conducted at two sites invaded by Chinese tallow. The Tulane

University’s F. Edward Hebert Riverside Research Center (HRRC) in Belle Chasse, Louisiana was chosen as an invaded bottomland hardwood forest (Fig. 2). The site is approximately 100 hectares in size and 1.22m above sea level (Wunderground 2015). The area bears evidence of drainage canals and most likely functioned as a cotton or sugar cane plantation during the 18th and 19th centuries due to its location along the Mississippi River (S. Darwin, personal communication). During World War II, The United States government owned the property and altered it to assist in wartime efforts. Tulane University acquired the property at the end of World

War II, and it has been allowed to grow unmanaged since then (Whitrock 2013). The overstory is comprised of native hardwood species including: Acer negundo, Acer rubrum, Carya illinoinensis, Celtis laevigata, Cornus, Liquidambar styraciflua, Prunus serotina, Quercus nigra,

Quercus texana, Quercus virginiana, Sambucus nigra, and Ulmus americana. Some areas include invasive Ligustrum lucidum and Triadica sebifera. Other notable species include Ilex vomitoria and Sabal minor. The understory is mostly comprised of invasive Ligustrum sinense

(Whitrock 2013).

7

Figure 2: Map of Tulane University's F. Edward Hebert Riverside Research Center

The Mississippi Sandhill Crane National Wildlife Refuge (MSCNWR) in Jackson County,

Mississippi, was chosen as the second sampling site and is representative of invaded longleaf pine savannah. The refuge encompasses 7,800 hectares over three separate units, divided into smaller management compartments (Fig. 3). The refuge was established in 1975 to protect the endangered Mississippi sandhill crane (Grus canadensis pulla) and restore the unique and disappearing habitat (USFWS 2007). The understory is species-rich and consists of grasses:

Aristida, Ctenium, Dicanthelium, Muhlenbergia, Schiazachyrium; sedges: Dichromena, Fuirena,

Rhynchospora, Scleria; rushes: Juncus; forbs: Aletris, Aster, Balduina, Bigelowia, Calopogon,

Carphephorus, Coreopsis, Eriocaulon, Eryngium, Eupatorium, Helianthus, Hypoxis,

Lachnanthes, Ludwigia, Lobelia, Lophiola, Phlox, Polygala, Rhexia, Sabatia, Solidago, Tofieldia,

Viola, Xyris, Zigadenus; and insectivorous plants: Drosera, Pinguicula, Sarracenia, Utricularia.

Larger plants include shrubs: Gaylussacia, Hypericum, and Vaccinium, and taller-growing species: Ilex, Clethra, Cyrilla, Lyonia, MyricaI, Pinus, and Taxodium (USFWS 2007).

8

Figure 3: Map of Mississippi Sandhill Crane National Wildlife Refuge units and compartments

Sampling design

To assess pollination mechanisms of Chinese tallow, exclusion experiments to test for self-fertilization and receptivity were performed at HRRC. Pollen traps were constructed to test for wind pollination in compartment G-02 of MSCNWR, and aerial netting of flower visitors was conducted at both sites. Experiments were performed in May and June of 2012 and 2013.

Self-fertilization survey

Chinese tallow is protogynous (McCormick 2005), which may reduce self-pollination. To determine if self-pollination occurs under natural conditions, I bagged 20 unopened buds on four trees at HRRC in late May 2012. Fine nylon mesh was secured around twigs approximately 4 cm below from the base of the inflorescence and sealed with wire (Fig. 4). The bags remained on

9 inflorescences the entire flowering season, and when removed, the peduncle was examined for capsules.

Figure 4: Bagged inflorescence

Receptivity survey

To test daily stigmatic receptivity, 20 immature inflorescences were bagged on three test trees at HRRC as described in the self-fertilization survey. Four bags from each tree were systematically removed for two days and then replaced and tagged with exposure dates, beginning on the day of anthesis and ending at 10 days post-anthesis (Fig. 5). The bags were visually inspected for fruit development every 10 days after the exposure trial and removed at the end of the flowering season.

10

Figure 5: Tagged inflorescence post- exposure Figure 6: Pollen trap

Airborne pollen count

To determine if Chinese tallow is capable of wind pollination, we surveyed for wind-born pollen using pollen traps made of standard microscope slides coated in petroleum jelly as outlined by Kearns and Inouye (1993). Slides were mounted on rings made from PVC pipe 7.5 cm in diameter and cut one cm thick, which attached to a length of PVC pipe 2.5 cm in diameter secured approximately 30 cm from the ground (Fig. 6). In June 2013, at the height of flowering, we placed traps around two trees at MSCNWR at 1, 4, and 8-meter intervals in the four cardinal directions. Traps were open for 24 hours, and subsequently the slides were removed and placed in individual plastic bags for transportation to the lab for analysis.

Insect pollination survey

Insect pollination was assessed using aerial netting of flower visiting insects. A flower- visiting insect was defined as any insect that made contact with an inflorescence in anthesis. We sampled trees for five minutes each, sweeping at all flower visiting insects within reach. In May and June 2012, we sampled 7 trees at HRRC. We revisited three trees that exhibited an extended flowering period, for a total of 10 samples. In June 2013, we sampled 6 trees at HRRC,

11 revisiting one, for a total of 7 samples, and at MSCNWR, we sampled 8 trees, revisiting 2, for a total of 10 samples. Insects were stored in vials containing 70% ethyl alcohol as collected.

Insect identification

Insects were identified morphologically to the lowest taxonomic level possible; all were identified to family, 80% to genus and 54% to species. Key references included Arnett et al.

2000; Arnett and Thomas 2002; Buck et al. 2008; McAlpine et al. 1981, 1987; Mitchell 1960,

1962; and Slater and Baranowski 1978.

Pollen identification

Pollen was identified morphologically using light microscopy at 400x and compared to images from Lieux (1975) and Trigg at al. (2013). For flower visitor pollen samples, I gently removed external pollen from insects using insect pins. Pollen was put onto glass slides, and I sealed cover slips using clear nail polish. Flower visitor slides and pollen trap slides were inspected methodically as outlined by Jones (2012). Chinese tallow pollen was identified by its tricolporate shape and large 32-43μm diameter (Dustmann and Von Der Ohe 1993, Lieux 1975).

I recorded the number of Chinese tallow versus other pollen grains in five field views of each slide.

Statistical analysis

All statistical analysis was performed in SYSTAT version 13, except Chi-squared tests, which were run in R version 2.13.1. Receptivity data was analyzed using a repeated measured

ANOVA of fruit set among trees over time. Airborne pollen was analyzed with regression analysis on the number of tallow and non-tallow pollen grains collected on pollen traps at

12 varying distances. External pollen loads were analyzed using an ANOVA on the arcsine-square root transformed proportions with Tukey’s HSD post hoc analysis. To investigate if site, particularly the floral communities invaded, affected the presence of orders, families, or genera of insects, we ran Pearson’s Chi-squared tests (푥2) using Monte Carlo simulations with p-values based on 999 replicates.

13 Results

Self-fertilization survey

Of the 80 inflorescences bagged in the self-fertilization survey, 73 retained their bags throughout the duration of the study and were surveyed for fruit set. Although self-fertilized fruits were rare, at least one flower on each tree set fruit. An average of 9.8 ± 4.8% of inflorescences set fruit. Inflorescences bore an average of three trilocular flowers capable of producing three seeds, and the mean seed set of the four trees was 1.38 ± 0.70% (Table 1).

Table 1: Proportion of fruits developed per test tree in self-fertilization survey

No Fruit 1 Fruit 2 Fruits % Fruits % Seeds

Tree 1 15 2 0 11.8 1.3 Tree 2 19 0 1 5.0 1.1 Tree 3 15 2 1 16.7 2.5 Tree 4 17 1 0 5.6 0.6 Average 9.8 ± 4.8 1.38 ± 0.70

Receptivity survey

In the receptivity experiment all test inflorescences set at least one fruit. Average fruit set of the three test trees was 28.9 ± 6.5% and varied from a high of 36.1 to a low of 23.3%. Number of fruits set differed significantly among trees (F2,9 = 8.123, p = 0.010), with tree #2 (36.1%) out- producing the others (Table 2). Receptivity of flowers did not vary over time (Day effect, F4,36 =

0.841, p = 0.509), and was similar over time for all trees (Day x Tree interaction; F8,36 = 0.380, p

= 0.924).

14

Table 2: Repeated measured ANOVA of fruit set among trees over time

Between Subjects Within Subjects Source Tree Day exposed Day x Tree F-ratio 8.123 1 0.841 2 0.380 3 P value 0.010 0.509 0.924 1: df = 2,9 2: df = 4,36 3 df = 8,36

Airborne pollen count

While Chinese tallow pollen was found on pollen traps, it comprised a small fraction of all pollen. Only 1% of pollen on slides was attributed to Chinese tallow (Table 3), while the rest was from other species. Regression analysis showed that abundance of Chinese tallow pollen in microscope fields decreased significantly with distance from the tree (Y = -0.11X + 0.79; r2 =

0.59; p < 0.001) (Fig. 7). In contrast, abundance of other pollen types did not vary significantly with distance from the target tree (Y = 0.05X + 24.1; r2 = 0.003; p = 0.817) (Fig. 7).

Table 3: Number of tallow and non-tallow pollen grains per microscope field for two trees, collected on pollen traps at varying distances

Tree 1 Tree 2

Distance (m) Tallow Non-tallow Tallow Non-tallow 1 0.6 ± 0.24 23 ± 2.5 0.9 ± 0.36 25 ± 2.7 4 0.2 ± 0.14 25.8 ± 1.9 0.3 ± 0.22 23.6 ± 3.9 8 0 24.2 ± 1.2 0 25.2 ± 3.3

15

Figure 7: Number of pollen grains per microscope field vs. distance from source tree. Tallow pollen regression: Y = -0.11X + 0.79; r2 = 0.59; p < 0.001. Non-tallow pollen regression: Y = 0.05X + 24.1; r2 = 0.003; p = 0.817

Insect pollination survey and identification

178 individual insects were collected on tallow trees; 35 were removed from the data set as either too degraded to identify, or incidental visitors unlikely to pollinate tallow flowers (4

Lepidoptera) and non-pollinating arthropods (arachnids). Of the remaining 143 individuals, 94 were collected at HRRC and 49 at MSCNWR. The majority were Hymenoptera (71%), with the others being Diptera (13%), Coleoptera (10%), and Hemiptera (6%). Within the order

Hymenoptera, 5 families were represented with the majority being Apidae at 70%. The other families included Vespidae (14%), Formicidae (10%), Halictidae (6%), and Ichneumonidae

(<1%). Apidae was represented by 5 species: Apis mellifera (51), Melissodes bimaculata (13),

16 Xylocopa virginica (5), X. micans (1), and a single undetermined Xylocopa species. Halictids were represented by the species Augochloropsis metallica (4) and Augochlora pura (2).

Using Pearson’s Chi-squared test with a simulated p-value (based on 999 replicates) we analyzed whether the difference in ecosystem, particularly the floral communities that were invaded, affected the presence of particular orders, families, or genera of insects. We then analyzed if site affected the families found in each of the four orders found in our study (Table 4).

Each variable showed a significant difference between sites except when families of

Hymenoptera were compared (p = 0.467).

Table 4: Comparison of abundance of taxa visiting Chinese tallow flowers at two sites on the central Gulf Coast. P- values are of Pearson's Chi-squared test with Monte Carlo simulations.

p-value p-value

Orders 0.001 Hemiptera 0.004 Families 0.001 Hymenoptera 0.467 Genera 0.001 Hymenoptera without Apis 0.001 Coleoptera 0.003 Apidae 0.087 Diptera 0.001 Apidae without Apis 0.001

33 species were collected at the HRRC, 15 being from the order Hymenoptera and making up the bulk of the samples. More than half of the Hymenoptera collected (62%) were bees from 6 species across 2 families; 82% were Apidae and 18% Halictidea. M. bimaculata represented 46%, A. mellifera 32%, X. virginica 18%, and X. micans 3.6% of Apidae collected. A. metallica made up 66% of the Halictids, with A. pura completing the other 33%. The 39 non-

Hymenopteran individuals came from 18 different species.

The MSCNWR only produced 7 species; 5 from the order Hymenoptera, with the majority being A. mellifera (42). Other Hymenopterans included 3 vespids, 1 Formicidae, and 1 unknown species of Xylocopa. The other 2 species were from the order Diptera.

17 Table 5: Species diversity by order and bee family at both sites

HRRC MSCNWR Order No. of Species Order No. of Species Hymenoptera 15 Hymenoptera 5 Coleoptera 7 Diptera 2 Hemiptera 6 Diptera 5 Bee Family No. of Species Bee Family No. of Species Apidae 4 Apidae 2 Halicidae 2

Pollen identification

We analyzed external pollen loads of Apis, Melissodes, both Xylocopa species, and both genera of Halictids combined. Chinese tallow pollen dominated loads of Apis (86%), Melissodes

(85%), and Halictids (79%), but made up only 14% of loads carried by Xylocopa (Table 5). An

ANOVA on the arcsine-square root transformed proportions showed the four groups carried significantly different proportions of tallow pollen in their pollen loads (F3, 31 = 11.8, p < 0.001).

Post-hoc comparisons showed no significant differences in the proportion of Chinese tallow pollen in pollen loads between Apis, Melissodes, and the Halictid species. The two Xylocopa species carried a significantly lower proportion of tallow pollen than all other groups (Tukey’s

HSD test p < 0.001 for all comparisons).

Table 6: Mean and standard deviation of 5 field views of pollen loads per group

n Tallow Non-tallow

Apis 12 7.233 ± 3.994 1.100 ± 1.864 Halictidae 6 2.400 ± 0.657 0.833 ± 2.041 Melissodes 12 6.583 ± 4.324 1.517 ± 1.478 Xylocopa 6 0.833 ± 0.612 6.000 ± 5.238

18 Discussion

My results suggest that Triadica sebifera on the Gulf Coast is strongly outcrossing and primarily bee pollinated. Seed production in pollinator exclusion experiments was only 5% of that in open-pollinated flowers, indicating the possibility of self fertilization if not considering the possibility of apomixis. The mean seed set of 29% in open-pollinated flowers was somewhat surprising given that flowers were receptive for up to 10 days after opening, and suggests that the study plants may have been pollinator-limited. Seed production in some populations has been estimated at over 100,000 per tree (Renne et al. 2000) and this level of production appears to be inconsistent with pollinator limitation. It is possible that visitation rates vary significantly among locations with pollinator community composition and abundance, or are strongly influenced by the density of flowering tallow trees. Our pollinator collections were intermittent and aimed primarily at establishing the identity of flower visitors rather than assessing rates of visitation.

Further studies comparing visitation rates in populations of different densities and in different locations would be of significant interest.

Chinese tallow pollen appears to be poorly dispersed by wind and unlikely to produce significant seed set under most conditions. Deposition of tallow pollen on sampling slides was low relative to that of other plant species, and dropped to essentially zero at 8 meters from the source. Wind dispersal of pollen could potentially produce significant seed set in dense stands of tallow, but its importance is likely to be minor compared to insect pollination in most populations.

External pollen loads of bee species show Apis, Melissodes, and Halictids visiting tallow with similar fidelity. Xylocopa pollen loads had greater diversity, showing more generalized

19 visitation. Our collection of bee species from the HRRC is consistent with common species previously found in bottomland hardwood forests (Hanula and Horn 2011, Ulyshen 2010), and suggests that common, native generalist flower visitors in this habitat can and do frequently visit

Chinese tallow. Although collection effort was greater at the HRRC, we collected fewer individual bees than at the MSCNWR. Despite lower numbers, bee species richness was higher at the HRRC.

The relatively low bee species diversity and the dominance of Apis among visitors to tallow trees at the MSCNWR is not consistent with bee assemblages previously found in longleaf pine savannah by Bartholomew (2004). Apis mellifera is known to have strong preferences for plants producing large amounts of pollen (Aronne et al. 2012), and may be preferentially foraging on Chinese tallow in this habitat to the exclusion of small, scattered native plants that produce only limited amounts of pollen. It is possible that interference competition from Apis reduced visitation rates of native bees to tallow trees at MSCNWR, as has been found in previous studies (Goulson 2003). Alternatively, solitary native bees such as Melissodes and

Augochlora are likely to have restricted flight distances compared to Apis mellifera (Gathmann and Tscharntke 2002) and may find it more profitable to exploit native herbaceous plants in longleaf pine savannahs near their nest sites (Peet and Allard 1993) than to fly long distances to exploit scattered Chinese tallow patches.

Our results do not support the idea that Triadica sebifera and Apis mellifera comprise an invasive mutualism that facilitated the spread of Chinese tallow in North America. While Apis dominated at MSCNWR, comprising 98% of all bee visitors, it made up only 26% of bee visitors at HRRC. In addition, Apis, Melissodes and Augochlora visitors all carried pollen loads equally dominated by tallow pollen, indicating that native bees visit tallow extensively. Because

20 Melissodes and Augochlora are comparable in size to Apis, we could not carry out pollinator exclusion experiments that might have determined if Apis was a more effective pollinator than native bees. However, the simple, open structure of Triadica flowers (Webster 1994) suggests that a wide variety of visitors, including native bees, should be effective pollinators.

Our results show that the pollination system of Triadica sebifera is well suited to a successful invader capable of at least a small amount of self-fertilization under natural conditions, and can potentially produce seed even under severe pollinator limitation. This would allow newly established populations to reproduce and potentially gain a foothold in a novel environment, even if insect visitation is low. Its ability to attract native pollinators suggests that, once established, this species would not be pollen limited, and this is consistent with the copious seed sets noted in other studies (Renne et al. 2000, Scheld and Cowles 1981). Overall, this species is far more likely to be limited by the physical environment, natural enemies, or competition from native plant species than by pollination services.

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29 Appendix

Receptivity Data

Table 7: Numbers of fruits developed in receptivity exclusion experiment

Day of Bag Removal Tree # 1 Tree # 2 Tree # 3 5/26/12 2 4 2 1 4 5 4 3 1 3 3 2 5/28/12 3 4 5 2 3 5 3 2 3 3 1 2 5/30/12 4 1 1 2 2 4 1 5 2 3 1 1 6/1/12 3 1 2 3 5 4 4 1 2 1 5 2 6/3/12 1 4 2 2 1 2 2 5 3 1 2 1

Insect Identification

Table 8: Arthropods collected (ms stands for morphospecies)

Date Time Capture # Order Family Genus Species 5/24/12 10:00 1 Hymenoptera Apidae Xylocopa virginica 5/24/12 10:00 2 Hymenoptera Apidae Xylocopa micans 5/24/12 10:00 3 Hymenoptera Apidae Apis mellifera 5/24/12 10:00 4 Hymenoptera Ichneumonidae – – 5/24/12 10:00 5 Coleoptera Oedemeridae Oxacis – 5/24/12 10:00 6 Coleoptera Coccinellidae Harmonia – 6/4/12 13:00 1 Hymenoptera Apidae Melissodes bimaculata 6/4/12 13:00 2 Hymenoptera Apidae Melissodes bimaculata 6/4/12 13:00 3 Hymenoptera Apidae Melissodes bimaculata 6/4/12 13:00 4 Hymenoptera Apidae Melissodes bimaculata 6/4/12 13:00 5 Diptera Syrphidae Palpada – 6/4/12 13:00 6 Diptera Syrphidae Palpada – 6/4/12 13:00 7 Hymenoptera Vespidae Polistes ms1 6/4/12 13:00 8 Hymenoptera Apidae Apis mellifera 6/4/12 13:00 9 Hymenoptera Apidae Apis mellifera 6/6/12 12:00 5 Hymenoptera Apidae Apis mellifera 6/6/12 12:00 7 Coleoptera Scarabaeidae Euphoria – 6/6/12 12:00 8 Hemiptera Pentatomidae Euschistus – 6/6/12 12:00 9 Coleoptera Oedemeridae Oxacis – 6/6/12 12:00 10 Hymenoptera Apidae Apis mellifera 6/6/12 12:00 11 Hemiptera Pentatomidae Euschistus –

30 (table continued) 6/6/12 12:00 14 Coleoptera Coccinellidae Harmonia – 6/6/12 12:00 15 Coleoptera Oedemeridae Oxacis – 6/6/12 13:00 1 Hymenoptera Halictidae Augochloropsis metallica 6/6/12 13:00 2 Coleoptera Chrysomelidae Paria – 6/6/12 13:00 3 Hymenoptera Apidae Apis mellifera 6/6/12 13:00 5 Hymenoptera Apidae Apis mellifera 6/6/12 13:00 8 Coleoptera Histeridae Paromalus – 6/6/12 13:00 9 Hymenoptera Apidae Apis mellifera 6/13/12 13:00 3 Hymenoptera Vespidae – ms2 6/13/12 13:00 4 Coleoptera Elateridae Glyphonyx – 6/13/12 13:00 5 Hymenoptera Vespidae – ms3 6/13/12 13:00 6 Hymenoptera Apidae Melissodes bimaculata 6/13/12 13:00 7 Hymenoptera Apidae Melissodes bimaculata 6/15/12 13:00 2 Hymenoptera Vespidae Zethus ms2 6/15/12 13:00 4 Hymenoptera Apidae Apis mellifera 6/15/12 13:00 6 Diptera Syrphidae Palpada – 6/15/12 13:00 7 Hemiptera Largidae Largus – 6/15/12 13:00 8 Hemiptera Largidae Largus – 6/15/12 13:00 9 Coleoptera Elateridae Glyphonyx – 6/15/12 14:00 1 Hemiptera Reduviidae Zelus – 6/15/12 14:00 2 Diptera Sarcophagidae Tylomyia – 6/15/12 14:00 3 Diptera Dolichopodidae Chrysotus – 6/15/12 14:00 4 Diptera Sarcophagidae Tylomyia – 6/15/12 14:00 5 Diptera Sarcophagidae Tylomyia – 6/15/12 14:00 7 Diptera Sarcophagidae Tylomyia – 6/15/12 14:00 8 Diptera Sarcophagidae Tylomyia – 6/15/12 14:00 9 Diptera Dolichopodidae Chrysotus – 6/15/12 14:00 10 Hymenoptera Formicidae – ms1 6/15/12 14:00 11 Hemiptera Rhopalidae Arhyssus – 6/15/12 14:00 12 Hymenoptera Formicidae – ms1 6/15/12 14:00 13 Hymenoptera Vespidae – ms3 6/18/12 15:00 1 Hymenoptera Apidae Melissodes bimaculata 6/18/12 15:00 2 Diptera Tachinidae – – 6/18/12 15:00 3 Hymenoptera Vespidae – ms4 6/18/12 15:00 4 Diptera Tachinidae – – 6/18/12 15:00 5 Hymenoptera Vespidae – ms5 6/18/12 15:00 6 Coleoptera Elateridae Glyphonyx – 6/18/12 15:00 7 Hymenoptera Vespidae – ms6 6/18/12 15:00 8 Diptera Syrphidae Palpada – 6/18/12 15:00 9 Coleoptera Scarabaeidae Trigonopeltastes – 6/18/12 15:00 13 Diptera Syrphidae Palpada – 6/24/12 18:00 1 Diptera Asilidae Ommatius –

31 (table continued) 6/24/12 18:00 2 Hymenoptera Formicidae – ms1 6/24/12 18:00 3 Diptera Tachinidae – – 6/27/12 11:00 1 Hymenoptera Formicidae – ms2 6/12/13 11:00 1 Hymenoptera Halictidae Augochloropsis metallica 6/12/13 11:00 2 Hymenoptera Halictidae Augochloropsis metallica 6/12/13 11:00 3 Hymenoptera Halictidae Augochloropsis metallica 6/12/13 11:00 4 Hymenoptera Vespidae – ms6 6/12/13 11:00 5 Hymenoptera Apidae Melissodes bimaculata 6/12/13 12:00 1 Hymenoptera Formicidae – ms1 6/12/13 12:00 2 Hemiptera Miridae Eustictus – 6/12/13 12:00 3 Hymenoptera Formicidae – ms1 6/14/13 12:00 1 Hymenoptera Apidae Xylocopa ms1 6/14/13 12:00 2 Hymenoptera Apidae Apis mellifera 6/14/13 12:00 3 Hymenoptera Apidae Apis mellifera 6/14/13 12:00 4 Hymenoptera Apidae Apis mellifera 6/14/13 12:00 5 Hymenoptera Apidae Apis mellifera 6/14/13 12:30 1 Hymenoptera Apidae Apis mellifera 6/14/13 12:30 2 Hymenoptera Apidae Apis mellifera 6/14/13 12:30 3 Hymenoptera Apidae Apis mellifera 6/14/13 12:30 4 Hymenoptera Apidae Apis mellifera 6/14/13 12:30 5 Hymenoptera Apidae Apis mellifera 6/14/13 12:30 6 Hymenoptera Apidae Apis mellifera 6/14/13 13:00 1 Hymenoptera Vespidae – ms6 6/14/13 13:00 2 Hymenoptera Apidae Apis mellifera 6/14/13 13:00 3 Hymenoptera Apidae Apis mellifera 6/14/13 13:00 4 Hymenoptera Apidae Apis mellifera 6/14/13 13:00 5 Hymenoptera Apidae Apis mellifera 6/19/13 12:00 1 Hemiptera Miridae Eustictus – 6/19/13 12:00 2 Hymenoptera Formicidae – ms2 6/19/13 12:00 8 Hymenoptera Vespidae – ms6 6/19/13 12:00 9 Hymenoptera Apidae Xylocopa virginica 6/19/13 12:00 10 Hymenoptera Apidae Melissodes bimaculata 6/19/13 12:00 11 Hymenoptera Apidae Melissodes bimaculata 6/19/13 12:00 12 Hymenoptera Apidae Melissodes bimaculata 6/19/13 12:00 13 Hymenoptera Apidae Melissodes bimaculata 6/19/13 12:00 14 Coleoptera Coccinellidae Harmonia – 6/19/13 12:00 15 Hemiptera Pentatomidae Cosmopepla – 6/19/13 12:00 16 Hymenoptera Apidae Xylocopa virginica 6/19/13 13:00 1 Hymenoptera Formicidae – ms2 6/19/13 13:00 3 Hymenoptera Apidae Xylocopa virginica 6/21/13 10:00 1 Hymenoptera Apidae Apis mellifera 6/21/13 10:00 2 Hymenoptera Apidae Apis mellifera

32 (table continued) 6/21/13 10:00 3 Hymenoptera Apidae Apis mellifera 6/21/13 10:00 4 Hymenoptera Apidae Apis mellifera 6/21/13 10:00 5 Hymenoptera Apidae Apis mellifera 6/21/13 10:00 6 Hymenoptera Apidae Apis mellifera 6/21/13 10:00 7 Hymenoptera Apidae Apis mellifera 6/21/13 10:00 8 Hymenoptera Apidae Apis mellifera 6/21/13 10:15 1 Hymenoptera Apidae Apis mellifera 6/21/13 10:15 2 Hymenoptera Apidae Apis mellifera 6/21/13 10:15 3 Hymenoptera Apidae Apis mellifera 6/21/13 10:15 4 Hymenoptera Apidae Apis mellifera 6/21/13 10:15 5 Hymenoptera Apidae Apis mellifera 6/21/13 10:30 1 Hymenoptera Apidae Apis mellifera 6/21/13 10:30 2 Hymenoptera Apidae Apis mellifera 6/21/13 10:30 3 Hymenoptera Apidae Apis mellifera 6/21/13 10:30 4 Hymenoptera Apidae Apis mellifera 6/21/13 10:30 5 Hymenoptera Vespidae – ms7 6/21/13 10:30 6 Hymenoptera Apidae Apis mellifera 6/21/13 11:00 1 Hymenoptera Formicidae – ms2 6/21/13 11:00 2 Hymenoptera Vespidae – ms7 6/21/13 11:00 4 Hymenoptera Apidae Apis mellifera 6/21/13 11:00 5 Diptera Syrphidae Toxomerus – 6/21/13 11:15 6 Hymenoptera Apidae Apis mellifera 6/21/13 11:15 7 Hymenoptera Apidae Apis mellifera 6/21/13 11:15 8 Hymenoptera Apidae Apis mellifera 6/21/13 11:15 9 Hymenoptera Apidae Apis mellifera 6/21/13 11:30 1 Hymenoptera Apidae Apis mellifera 6/21/13 11:30 2 Diptera – – – 6/21/13 11:30 3 Hymenoptera Apidae Apis mellifera 6/21/13 11:30 5 Hymenoptera Apidae Apis mellifera 6/21/13 11:30 6 Hymenoptera Apidae Apis mellifera 6/21/13 11:30 7 Hymenoptera Apidae Apis mellifera 6/25/13 14:00 1 Hymenoptera Halictidae Augochlora pura 6/25/13 14:00 3 Hymenoptera Formicidae – ms2 6/25/13 14:00 4 Hymenoptera Halictidae Augochlora pura 6/26/13 9:00 2 Coleoptera Scarabaeidae Trigonopeltastes – 6/26/13 9:00 3 Hymenoptera Apidae Melissodes bimaculata 6/26/13 9:00 4 Hymenoptera Vespidae – ms6 6/26/13 9:00 5 Hymenoptera Apidae Xylocopa virginica

33 Vita

The author was born in New Orleans, Louisiana. She obtained her Bachelor of Science from the University of New Orleans in 2011. She joined the graduate program to pursue a Master of Science in Biological Sciences under the advisement of Dr. Jerome Howard, which she completed in 2016.

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